@article{beza-beza_wiegmann_ware_petersen_gunter_cole_schwarz_bertone_young_mikaelyan_2024, title={Chewing through challenges: Exploring the evolutionary pathways to wood-feeding in insects}, volume={3}, ISSN={["1521-1878"]}, url={https://doi.org/10.1002/bies.202300241}, DOI={10.1002/bies.202300241}, abstractNote={AbstractDecaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, from both saproxylophagous insects and their non‐saproxylophagous relatives, including new data from unexplored wood‐feeding insects, this Hypothesis paper discusses the broader phylogenetic context and potential adaptations necessary for this dietary specialization. The study proposes the “Detritivore‐First Hypothesis,” suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood.}, journal={BIOESSAYS}, author={Beza-Beza, Cristian F. and Wiegmann, Brian M. and Ware, Jessica A. and Petersen, Matt and Gunter, Nicole and Cole, Marissa E. and Schwarz, Melbert and Bertone, Matthew A. and Young, Daniel and Mikaelyan, Aram}, year={2024}, month={Mar} }
@article{osaki_nakazono_yabe_takata_mikaelyan_2024, title={Fight, retreat, repeat: The male–male agonistic behavior in the wood‐feeding cockroach, Panesthia angustipennis spadica (Dictyoptera: Blattodea: Blaberidae)}, url={https://doi.org/10.1002/ece3.70319}, DOI={10.1002/ece3.70319}, abstractNote={Competition is one of the most critical factors affecting animal behaviors. Aggressive interactions are central to acquiring resources or mating partners. Agonistic behavior is more common among males than females. Although laboratory observations of these behaviors give detailed descriptions under controlled conditions, field observations without human intervention are required because those supply information that provides insights into their function. In this paper, we report on the field observation and auxiliary laboratory experiments of male-male agonistic behavior of a wood-feeding cockroach,}, journal={Ecology and Evolution}, author={Osaki, Haruka and Nakazono, Tomohiro and Yabe, Kiyotaka and Takata, Mamoru and Mikaelyan, Aram}, year={2024}, month={Oct} }
@article{ashbrook_schwarz_schal_mikaelyan_2024, title={Lethal Disruption of the Symbiotic Gut Community in Eastern Subterranean Termite Caused by Boric Acid}, url={https://doi.org/10.1101/2024.06.26.600876}, DOI={10.1101/2024.06.26.600876}, abstractNote={The Eastern subterranean termite, Reticulitermes flavipes (Kollar), is a significant pest, causing extensive damage to structures that amount to substantial economic losses. Traditional termite control methods have utilized boric acid, known for its broad-spectrum insecticidal properties, yet its impact on termite gut microbiomes and the implications of such effects remain understudied. Our study evaluates the dose-dependent mortality of R. flavipes upon being provided boric acid treated filter papers and investigates the resulting dysbiosis within the termite gut microbiome. Consistent with reports from other insects, mortality increased in a dose-dependent manner, with the highest boric acid concentration (203.7 ug/cm2 of filter paper) significantly reducing termite survival. 16S rRNA gene sequencing of the gut microbiome revealed notable shifts in composition, indicating boric acid-induced dysbiosis. Aside from an overall decrease in microbial diversity, the relative abundance of some symbionts essential for termite nutrition decreased in response to higher boric acid concentrations, while several putative pathogens increased. Our findings extend the understanding of boric acid's mode of action in termites, emphasizing its effect beyond direct toxicity to include significant microbiome modulation that can have dire effects on termite biology. Considering its potential to induce dysbiosis and potentially augment the effectiveness of entomopathogens, our study supports the continued use of boric acid and related compounds for termite-resistant treatments for wood.}, author={Ashbrook, Aaron R. and Schwarz, Melbert and Schal, Coby and Mikaelyan, Aram}, year={2024}, month={Jun} }
@article{ashbrook_schwarz_schal_mikaelyan_2024, title={Lethal disruption of the bacterial gut community in Eastern subterranean termite caused by boric acid}, volume={10}, ISSN={["1938-291X"]}, url={https://doi.org/10.1093/jee/toae221}, DOI={10.1093/jee/toae221}, abstractNote={Abstract The Eastern subterranean termite, Reticulitermes flavipes (Kollar) (Blattodea: Rhinotermitidae), is a significant pest, causing extensive damage to structures that amount to substantial economic losses. Boric acid is widely used for wood preservation due to its stability and broad-spectrum insecticidal properties, yet its impact on termite gut microbiomes and the implications of such effects remain understudied. Our study evaluates the dose-dependent mortality of R. flavipes upon being provided boric acid treated filter papers and investigates the resulting dysbiosis within the termite gut microbiome. Consistent with reports from other insects, mortality increased in a dose-dependent manner, with the highest boric acid concentration (203.7 µg/cm2 of filter paper) significantly reducing termite survival. 16S rRNA gene sequencing of the gut bacterial microbiome revealed notable shifts in composition, indicating boric acid-induced dysbiosis. Aside from an overall decrease in bacterial diversity, the relative abundance of some symbionts essential for termite nutrition decreased in response to higher boric acid concentrations, while several opportunistic pathogens increased. Our findings extend the understanding of boric acid’s mode of action in termites, emphasizing its ability to significantly modulate the bacterial symbiont community, which can have dire effects on termite biology. Considering its ability to protect wood from further termite consumption, our study supports the continued use of boric acid and related compounds for termite-resistant treatments for wood.}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Ashbrook, Aaron R. and Schwarz, Melbert and Schal, Coby and Mikaelyan, Aram}, editor={Husseneder, ClaudiaEditor}, year={2024}, month={Oct} }
@article{wilkins_rapciak_goller_weintraub_mikaelyan_2024, title={Scaling the wall: overcoming barriers to STEM knowledge mobilization}, volume={9}, ISSN={["2297-900X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85190093976&partnerID=MN8TOARS}, DOI={10.3389/fcomm.2024.1366207}, abstractNote={Improving science literacy is crucial amidst global challenges like climate change, emerging diseases, AI, and rampant disinformation. This is vital not only for future STEM generations but for all, to make informed decisions. Informal science communication efforts such as podcasts, popular science articles, and museum events are an essential part of the infrastructure for mobilizing knowledge and nurturing science literacy. However, in this Perspective, we emphasize the need to grow our capacity for STEM outreach in the formal K-12 classroom. While the majority of informal outreach mechanisms require audience members to seek out content, classrooms include those hard-to-reach target audiences that are not already STEM-engaged. We contrast the multitude of resources that have been developed to support informal outreach in recent decades with a relative paucity of such efforts in the K-12 formal classroom realm. We advocate for a more balanced deployment of resources and efforts between these two vital components of our knowledge mobilization and STEM engagement infrastructure. In particular, we highlight the key role of K-12 teachers as conduits for knowledge dissemination and the need for greater collaboration between scientists and teachers at individual and organizational levels. We also advocate for greater collaboration across programs in both the informal and formal outreach space, and dedicated effort to construct dissemination networks to share outreach materials at scale across disparate programs. The aim of our piece is to generate discussion about how we might refocus goals, funding mechanisms, and policies to grow the science-engaged society necessary to confront future challenges.}, journal={FRONTIERS IN COMMUNICATION}, author={Wilkins, Matthew R. and Rapciak, Stephanie E. and Goller, Carlos C. and Weintraub, Jory and Mikaelyan, Aram}, year={2024}, month={Mar} }
@article{wang_mikaelyan_coates_lorenzen_2024, title={The Genome of Arsenophonus sp. and Its Potential Contribution in the Corn Planthopper, Peregrinus maidis}, volume={15}, ISSN={["2075-4450"]}, url={https://doi.org/10.3390/insects15020113}, DOI={10.3390/insects15020113}, abstractNote={The co-evolution between symbionts and their insect hosts has led to intricate functional interdependencies. Advances in DNA-sequencing technologies have not only reduced the cost of sequencing but, with the advent of highly accurate long-read methods, have also enabled facile genome assembly even using mixed genomic input, thereby allowing us to more easily assess the contribution of symbionts to their insect hosts. In this study, genomic data recently generated from Peregrinus maidis was used to assemble the genome of a bacterial symbiont, Pm Arsenophonus sp. This ~4.9-Mb assembly is one of the largest Arsenophonus genomes reported to date. The Benchmarking Universal Single-Copy Orthologs (BUSCO) result indicates that this Pm Arsenophonus assembly has a high degree of completeness, with 96% of the single-copy Enterobacterales orthologs found. The identity of the Pm Arsenophonus sp. was further confirmed by phylogenetic analysis. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicates a major contribution by Pm Arsenophonus sp. to the biosynthesis of B vitamins and essential amino acids in P. maidis, where threonine and lysine production is carried out solely by Pm Arsenophonus sp. This study not only provides deeper insights into the evolutionary relationships between symbionts and their insect hosts, but also adds to our understanding of insect biology, potentially guiding the development of novel pest control methods.}, number={2}, journal={INSECTS}, author={Wang, Yu-Hui and Mikaelyan, Aram and Coates, Brad S. and Lorenzen, Marce}, year={2024}, month={Feb} }
@article{amanor_acheampong_luke_smith_ryan_kermode_morris_cornelius_eziah_fening_et al._2024, title={Viability and virulence of freeze-dried Beauveria bassiana, Metarhizium acridum, and Hirsutella thompsonii isolates under non-refrigerated conditions in Ghana}, volume={3}, ISSN={["1360-0478"]}, DOI={10.1080/09583157.2024.2332337}, abstractNote={The necessity of cold storage for mycoinsecticides poses a logistical challenge in tropical Africa, where maintaining consistent refrigeration is a major obstacle. To investigate alternative preservation methods, our study evaluates conidial-based freeze-dried formulations of Beauveria bassiana (IMI 389521), Metarhizium acridum (IMI 330189), and mycelial-based freeze-dried formulations of Hirsutella thompsonii (IMI 327488 and IMI 391722). Propagules were cryoprotected with lactose, mannitol, and raffinose, encapsulated, and freeze-dried in plastic and glass vials. Bioformulations in glass vials were cryoprotected with mannitol only. Viability (CFU/g each day) of bioformulations, following 16-weeks-storage, and their virulence (at 1 × 107 conidia mL−1 in six days) against key pests of maize and cassava in Africa (larger grain borer, variegated grasshopper and cassava green mite) were determined under ambient laboratory conditions in Ghana. Our results show that non-freeze-dried conidia of B. bassiana and M. acridum had significantly higher viability and efficacy than freeze-dried versions, when stored under non-refrigerated conditions (averaging 27.7°C, 78.8% RH). Freeze-dried H. thompsonii mycelia were neither viable nor virulent against cassava green mite. Freeze-dried B. bassiana and M. acridum in plastic vials remained viable for 12 weeks, while in glass vials they were viable for seven weeks. Freeze-dried B. bassiana in both plastic and glass vials caused 38–43% mortality in larger grain borer, and M. acridum caused 45–82% mortality in variegated grasshopper. Further, conidia cryoprotected with lactose had significantly higher viability and mortality than raffinose and mannitol. Our research contributes to mycoinsecticide development, particularly in the context of storage and application challenges in tropical climates.}, journal={BIOCONTROL SCIENCE AND TECHNOLOGY}, author={Amanor, Gabriel Tetteh and Acheampong, Mavis Agyeiwaa and Luke, Belinda and Smith, David and Ryan, Mattew and Kermode, Anthony and Morris, John and Cornelius, Eric William and Eziah, Vincent Yao and Fening, Ken Okwae and et al.}, year={2024}, month={Mar} }
@article{carrijo_engel_chouvenc_gile_mikaelyan_dedeine_ware_haifig_arab_constantini_et al._2023, title={A call to termitologists: it is time to abandon the use of "lower" and "higher" termites}, volume={8}, ISSN={["1420-9098"]}, url={https://doi.org/10.1007/s00040-023-00929-0}, DOI={10.1007/s00040-023-00929-0}, journal={INSECTES SOCIAUX}, author={Carrijo, T. F. and Engel, M. S. and Chouvenc, T. and Gile, G. H. and Mikaelyan, A. and Dedeine, F. and Ware, J. L. and Haifig, I. and Arab, A. and Constantini, J. P. and et al.}, year={2023}, month={Aug} }
@article{beza-beza_wiegmann_ware_petersen_gunter_cole_schwarz_bertone_young_mikaelyan_2023, title={Chewing Through Challenges: Exploring the Evolutionary Pathways to Wood-Feeding in Insects}, url={https://doi.org/10.1101/2023.12.27.573094}, DOI={10.1101/2023.12.27.573094}, abstractNote={AbstractDecaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, encompassing both previously published datasets and newly generated data, from both saproxylophagous insects and their non-saproxylophagous relatives, thisHypothesispaper discusses the broader phylogenetic context and potential morphological, physiological, and symbiotic adaptations necessary for this dietary specialization. The study proposes the “Detritivore-First Hypothesis,” suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood. The article aims to provide a deeper understanding of the macroevolutionary landscape and mechanisms underpinning the multiple origins and distribution of saproxylophagy in insects.}, author={Beza-Beza, Cristian F. and Wiegmann, Brian M. and Ware, Jessica A. and Petersen, Matt and Gunter, Nicole and Cole, Marissa E. and Schwarz, Melbert and Bertone, Matthew A. and Young, Daniel and Mikaelyan, Aram}, year={2023}, month={Dec} }
@article{schwarz_tokuda_osaki_mikaelyan_2023, title={Reevaluating Symbiotic Digestion in Cockroaches: Unveiling the Hindgut's Contribution to Digestion in Wood-Feeding Panesthiinae (Blaberidae)}, volume={14}, ISSN={["2075-4450"]}, url={https://doi.org/10.3390/insects14090768}, DOI={10.3390/insects14090768}, abstractNote={Cockroaches of the subfamily Panesthiinae (family Blaberidae) are among the few major groups of insects feeding on decayed wood. Despite having independently evolved the ability to thrive on this recalcitrant and nitrogen-limited resource, they are among the least studied of all wood-feeding insect groups. In the pursuit of unraveling their unique digestive strategies, we explored cellulase and xylanase activity in the crop, midgut, and hindgut lumens of Panesthia angustipennis and Salganea taiwanensis. Employing Percoll density gradient centrifugation, we further fractionated luminal fluid to elucidate how the activities in the gut lumen are further partitioned. Our findings challenge conventional wisdom, underscoring the significant contribution of the hindgut, which accounts for approximately one-fifth of cellulase and xylanase activity. Particle-associated enzymes, potentially of bacterial origin, dominate hindgut digestion, akin to symbiotic strategies observed in select termites and passalid beetles. Our study sheds new light on the digestive prowess of panesthiine cockroaches, providing invaluable insights into the evolution of wood-feeding insects and their remarkable adaptability to challenging, nutrient-poor substrates.}, number={9}, journal={INSECTS}, author={Schwarz, Melbert and Tokuda, Gaku and Osaki, Haruka and Mikaelyan, Aram}, year={2023}, month={Sep} }
@article{luke_acheampong_rangel_cornelius_asante_nboyine_eziah_fening_storm_jessop_et al._2023, title={The use of Beauveria bassiana for the control of the larger grain borer, Prostephanus truncatus, in stored maize: Semi-field trials in Ghana}, volume={127}, ISSN={["1878-6162"]}, url={http://dx.doi.org/10.1016/j.funbio.2023.08.004}, DOI={10.1016/j.funbio.2023.08.004}, abstractNote={Laboratory research in Ghana demonstrated the effectiveness of an isolate of Beauveria bassiana (IMI 389521) from the United Kingdom against the larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), a major pest of stored maize. The minimum effective concentration, following artificial infestation trials on maize, was between 109 and 1010 cfu/kg maize. Before moving out to village-level control, a major requirement was to determine if the product could effect control in artificially infested maize held under real environmental conditions in several locations in Ghana. Therefore, this study investigated the efficacy of formulated conidia of B. bassiana, IMI 389521, at two concentrations (1 × 109 and 3.16 × 109 cfu/kg maize) to control P. truncatus on stored maize kernels under semi-field conditions in Ghana. Maize (‘Obatanpa’ cultivar) kernels were treated with the formulated B. bassiana product and stored in polypropylene woven bags in cribs in Southern Ghana. After 24 h, one hundred adults of P. truncatus were placed into each bag containing the treated maize. Mortality and the percent of weight loss of kernels were assessed every two weeks for three months. The semi-field trials revealed the possibility of successfully controlling adult P. truncatus on maize kernels treated with B. bassiana at 3.16 × 109 cfu/kg maize. However, due to the minimal protection of kernels after four weeks, re-treating maize kernels after this period is recommended to ensure maximum protection during prolonged storage.}, number={12}, journal={FUNGAL BIOLOGY}, publisher={Elsevier BV}, author={Luke, Belinda and Acheampong, Mavis A. and Rangel, Drauzio E. N. and Cornelius, Eric W. and Asante, Stephen K. and Nboyine, Jerry A. and Eziah, Vincent Y. and Fening, Ken O. and Storm, Clare and Jessop, Nick and et al.}, year={2023}, month={Dec}, pages={1505–1511} }
@article{schwarz_beza-beza_mikaelyan_2023, title={Wood fibers are a crucial microhabitat for cellulose- and xylan- degrading bacteria in the hindgut of the wood-feeding beetle Odontotaenius disjunctus}, volume={14}, ISSN={["1664-302X"]}, url={http://dx.doi.org/10.3389/fmicb.2023.1173696}, DOI={10.3389/fmicb.2023.1173696}, abstractNote={IntroductionWood digestion in insects relies on the maintenance of a mosaic of numerous microhabitats, each colonized by distinct microbiomes. Understanding the division of digestive labor between these microhabitats- is central to understanding the physiology and evolution of symbiotic wood digestion. A microhabitat that has emerged to be of direct relevance to the process of lignocellulose digestion is the surface of ingested plant material. Wood particles in the guts of some termites are colonized by a specialized bacterial fiber-digesting microbiome, but whether this represents a widespread strategy among insect lineages that have independently evolved wood-feeding remains an open question.MethodsIn this study, we investigated the bacterial communities specifically associated with wood fibers in the gut of the passalid beetle Odontotaenius disjunctus. We developed a Percoll-based centrifugation method to isolate and enrich the wood particles from the anterior hindgut, allowing us to access the wood fibers and their associated microbiome. We then performed assays of enzyme activity and used short-read and long-read amplicon sequencing of the 16S rRNA gene to identify the composition of the fiber-associated microbiome.ResultsOur assays demonstrated that the anterior hindgut, which houses a majority of the bacterial load, is an important site for lignocellulose digestion. Wood particles enriched from the anterior hindgut contribute to a large proportion of the total enzyme activity. The sequencing revealed that O. disjunctus, like termites, harbors a distinct fiber-associated microbiome, but notably, its community is enriched in insect-specific groups of Lactococcus and Turicibacter.DiscussionOur study underscores the importance of microhabitats in fostering the complex symbiotic relationships between wood-feeding insects and their microbiomes. The discovery of distinct fiber-digesting symbionts in O. disjunctus, compared to termites, highlights the diverse evolutionary paths insects have taken to adapt to a challenging diet.}, journal={FRONTIERS IN MICROBIOLOGY}, publisher={Frontiers Media SA}, author={Schwarz, Melbert and Beza-Beza, Cristian. F. F. and Mikaelyan, Aram}, year={2023}, month={Jun} }
@article{ashbrook_mikaelyan_schal_2022, title={Comparative Efficacy of a Fungal Entomopathogen with a Broad Host Range against Two Human-Associated Pests}, volume={13}, ISSN={["2075-4450"]}, url={https://doi.org/10.3390/insects13090774}, DOI={10.3390/insects13090774}, abstractNote={The ability of a fungal entomopathogen to infect an insect depends on a variety of factors, including strain, host, and environmental conditions. Similarly, an insect’s ability to prevent fungal infection is dependent on its biology, environment, and evolutionary history. Synanthropic pests have adapted to thrive in the indoor environment, yet they arose from divergent evolutionary lineages and occupy different feeding guilds. The hematophagous bed bug (Cimex lectularius) and omnivorous German cockroach (Blattella germanica) are highly successful indoors, but have evolved different physiological and behavioral adaptations to cope with the human-built environment, some of which also reduce the efficacy of fungal biopesticides. In order to gain greater insight into the host barriers that prevent or constrain fungal infection in bed bugs and German cockroaches, we tested different doses of Beauveria bassiana GHA through surface contact, topical application, feeding, and injection. Bed bugs were generally more susceptible to infection by B. bassiana with the mode of delivery having a significant impact on infectivity. The German cockroach was highly resilient to infection, requiring high doses of fungal conidia (>8.8 × 104) delivered by injection into the hemocoel to cause mortality. Mortality occurred much faster in both insect species after exposure to surfaces dusted with dry conidia than surfaces treated with conidia suspended in water or oil. These findings highlight the importance of developing innovative delivery techniques to enhance fungal entomopathogens against bed bugs and cockroaches.}, number={9}, journal={INSECTS}, author={Ashbrook, Aaron R. and Mikaelyan, Aram and Schal, Coby}, year={2022}, month={Sep} }
@article{mikaelyan_2021, title={Beating Them with Their Own Stick-Tick Uses Amidase of Bacterial Origin as Part of Its Immune Arsenal}, volume={29}, ISSN={["1934-6069"]}, url={https://doi.org/10.1016/j.chom.2020.12.019}, DOI={10.1016/j.chom.2020.12.019}, abstractNote={As vectors of microbial diseases in vertebrates, ticks are excellent at regulating bacterial proliferation in and around them. In a recent issue of Cell, Hayes et al., 2020Hayes B.M. Radkov A.D. Yarza F. Flores S. Kim J. Zhao Z. Lexa K.W. Marnin L. Biboy J. Bowcut V. et al.Ticks resist skin commensals with immune factor of bacterial origin.Cell. 2020; 183: 1562-1571.e12Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar reveal acarid toxins of bacterial origin that help eliminate microbes that are pathogenic to black-legged ticks but commensal to their vertebrate hosts.}, number={1}, journal={CELL HOST & MICROBE}, author={Mikaelyan, Aram}, year={2021}, month={Jan}, pages={1–3} }
@article{cross_leigh_hatmaker_mikaelyan_miller_bordenstein_2021, title={Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown}, volume={6}, ISSN={["2379-5077"]}, DOI={10.1128/mSystems.01342-20}, abstractNote={Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis.}, number={2}, journal={MSYSTEMS}, author={Cross, Karissa L. and Leigh, Brittany A. and Hatmaker, E. Anne and Mikaelyan, Aram and Miller, Asia K. and Bordenstein, Seth R.}, year={2021}, month={Apr} }
@article{cross_leigh_hatmaker_mikaelyan_miller_bordenstein_2021, title={Genomes of gut bacteria fromNasoniawasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown}, url={https://doi.org/10.1101/2021.02.13.431100}, DOI={10.1101/2021.02.13.431100}, abstractNote={ABSTRACTPhylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacteria in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterial-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterial-assisted lethality in hybrids are: (i) Do the Nasonia bacterial genomes differ from other animal isolates and (ii) Are the hybrid bacterial genomes the same as those in the parental species? Here we report the cultivation, whole genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and when grown in co-culture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent to pathogenic, human-associates strains. Proteus mirabilis from N. vitripennis, N. giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown.IMPORTANCEAnimal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely-related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species or host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus that contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.}, author={Cross, Karissa L. and Leigh, Brittany A. and Hatmaker, E. Anne and Mikaelyan, Aram and Miller, Asia K. and Bordenstein, Seth R.}, year={2021}, month={Feb} }
@article{cole_ceja-navarro_mikaelyan_2021, title={The power of poop: Defecation behaviors and social hygiene in insects}, volume={17}, ISSN={["1553-7374"]}, url={https://doi.org/10.1371/journal.ppat.1009964}, DOI={10.1371/journal.ppat.1009964}, abstractNote={1 Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina, United States of America, 2 Joint BioEnergy Institute, Emeryville, California, United States of America, 3 Bioengineering and Biomedical Sciences Department, Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America, 4 Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, California, United States of America}, number={10}, journal={PLOS PATHOGENS}, author={Cole, Marissa E. and Ceja-Navarro, Javier A. and Mikaelyan, Aram}, editor={Jabra-Rizk, Mary AnnEditor}, year={2021}, month={Oct} }
@article{lampert_mikaelyan_brune_2019, title={Diet is not the primary driver of bacterial community structure in the gut of litter-feeding cockroaches}, volume={19}, ISSN={["1471-2180"]}, url={https://europepmc.org/articles/PMC6864750}, DOI={10.1186/s12866-019-1601-9}, abstractNote={AbstractBackgroundDiet is a major determinant of bacterial community structure in termite guts, but evidence of its importance in the closely related cockroaches is conflicting. Here, we investigated the ecological drivers of the bacterial gut microbiota in cockroaches that feed on lignocellulosic leaf litter.ResultsThe physicochemical conditions determined with microsensors in the guts ofErgaula capucina,Pycnoscelus surinamensis, andByrsotria rothiwere similar to those reported for both wood-feeding and omnivorous cockroaches. All gut compartments were anoxic at the center and showed a slightly acidic to neutral pH and variable but slightly reducing conditions. Hydrogen accumulated only in the crop ofB. rothi. High-throughput amplicon sequencing of bacterial 16S rRNA genes documented that community structure in individual gut compartments correlated strongly with the respective microenvironmental conditions. A comparison of the hindgut microbiota of cockroaches and termites from different feeding groups revealed that the vast majority of the core taxa in cockroaches with a lignocellulosic diet were present also in omnivorous cockroaches but absent in wood-feeding higher termites.ConclusionOur results indicate that diet is not the primary driver of bacterial community structure in the gut of wood- and litter-feeding cockroaches. The high similarity to the gut microbiota of omnivorous cockroaches suggests that the dietary components that are actually digested do not differ fundamentally between feeding groups.}, number={1}, journal={BMC MICROBIOLOGY}, author={Lampert, Niclas and Mikaelyan, Aram and Brune, Andreas}, year={2019}, month={Oct} }
@article{tokuda_mikaelyan_fukui_matsuura_watanabe_fujishima_brune_2018, title={Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites}, volume={115}, ISSN={["0027-8424"]}, url={https://europepmc.org/articles/PMC6304966}, DOI={10.1073/pnas.1810550115}, abstractNote={
Symbiotic digestion of lignocellulose in wood-feeding higher termites (family Termitidae) is a two-step process that involves endogenous host cellulases secreted in the midgut and a dense bacterial community in the hindgut compartment. The genomes of the bacterial gut microbiota encode diverse cellulolytic and hemicellulolytic enzymes, but the contributions of host and bacterial symbionts to lignocellulose degradation remain ambiguous. Our previous studies of
Nasutitermes
spp. documented that the wood fibers in the hindgut paunch are consistently colonized not only by uncultured members of Fibrobacteres, which have been implicated in cellulose degradation, but also by unique lineages of Spirochaetes. Here, we demonstrate that the degradation of xylan, the major component of hemicellulose, is restricted to the hindgut compartment, where it is preferentially hydrolyzed over cellulose. Metatranscriptomic analysis documented that the majority of glycoside hydrolase (GH) transcripts expressed by the fiber-associated bacterial community belong to family GH11, which consists exclusively of xylanases. The substrate specificity was further confirmed by heterologous expression of the gene encoding the predominant homolog. Although the most abundant transcripts of GH11 in
Nasutitermes takasagoensis
were phylogenetically placed among their homologs of Firmicutes, immunofluorescence microscopy, compositional binning of metagenomics contigs, and the genomic context of the homologs indicated that they are encoded by Spirochaetes and were most likely obtained by horizontal gene transfer among the intestinal microbiota. The major role of spirochetes in xylan degradation is unprecedented and assigns the fiber-associated
Treponema
clades in the hindgut of wood-feeding higher termites a prominent part in the breakdown of hemicelluloses.
}, number={51}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Tokuda, Gaku and Mikaelyan, Aram and Fukui, Chiho and Matsuura, Yu and Watanabe, Hirofumi and Fujishima, Masahiro and Brune, Andreas}, year={2018}, month={Dec}, pages={E11996–E12004} }
@article{leigh_bordenstein_brooks_mikaelyan_bordenstein_2018, title={Finer-Scale Phylosymbiosis: Insights from Insect Viromes}, volume={3}, ISSN={["2379-5077"]}, url={https://europepmc.org/articles/PMC6299154}, DOI={10.1128/mSystems.00131-18}, abstractNote={
Viruses are the most abundant biological entity on the planet and interact with microbial communities with which they associate. The virome of animals is often dominated by bacterial viruses, known as bacteriophages or phages, which can (re)structure bacterial communities potentially vital to the animal host. Beta diversity relationships of animal-associated bacterial communities in laboratory and wild populations frequently parallel animal phylogenetic relationships, a pattern termed phylosymbiosis. However, little is known about whether viral communities also exhibit this eco-evolutionary pattern. Metagenomics of purified viruses from recently diverged species of
Nasonia
parasitoid wasps reared in the lab indicates for the first time that the community relationships of the virome can also exhibit complete phylosymbiosis. Therefore, viruses, particularly bacteriophages here, may also be influenced by animal evolutionary changes either directly or indirectly through the tripartite interactions among hosts, bacteria, and phage communities. Moreover, we report several new bacteriophage genomes from the common gut bacteria in
Nasonia
.
}, number={6}, journal={MSYSTEMS}, author={Leigh, Brittany A. and Bordenstein, Sarah R. and Brooks, Andrew W. and Mikaelyan, Aram and Bordenstein, Seth R.}, year={2018} }
@article{otani_zhukova_kone_costa_mikaelyan_sapountzis_poulsen_2019, title={Gut microbial compositions mirror caste-specific diets in a major lineage of social insects}, volume={11}, ISSN={["1758-2229"]}, url={https://europepmc.org/articles/PMC6850719}, DOI={10.1111/1758-2229.12728}, abstractNote={SummarySocial insects owe their ecological success to the division of labour between castes, but associations between microbial community compositions and castes with different tasks and diets have not been extensively explored. Fungus‐growing termites associate with fungi to degrade plant material, complemented by diverse gut microbial communities. Here, we explore whether division of labour and accompanying dietary differences between fungus‐growing termite castes are linked to gut bacterial community structure. Using amplicon sequencing, we characterize community compositions in sterile (worker and soldier) and reproductive (queen and king) termites and combine this with gut enzyme activities and microscopy to hypothesise sterile caste‐specific microbiota roles. Gut bacterial communities are structured primarily according to termite caste and genus and, in contrast to the observed rich and diverse sterile caste microbiotas, royal pair guts are dominated by few bacterial taxa, potentially reflecting their specialized uniform diet and unique lifestyle.}, number={2}, journal={ENVIRONMENTAL MICROBIOLOGY REPORTS}, author={Otani, Saria and Zhukova, Mariya and Kone, N'golo Abdoulaye and Costa, Rafael Rodrigues and Mikaelyan, Aram and Sapountzis, Panagiotis and Poulsen, Michael}, year={2019}, month={Apr}, pages={196–205} }
@article{pycnoscelus surinamensis cockroach gut microbiota respond consistently to a fungal diet without mirroring those of fungus-farming termites._2017, url={https://europepmc.org/articles/PMC5626473}, DOI={10.1371/journal.pone.0185745}, abstractNote={The gut microbiotas of cockroaches and termites play important roles in the symbiotic digestion of dietary components, such as lignocellulose. Diet has been proposed as a primary determinant of community structure within the gut, acting as a selection force to shape the diversity observed within this “bioreactor”, and as a key factor for the divergence of the termite gut microbiota from the omnivorous cockroach ancestor. The gut microbiota in most termites supports primarily the breakdown of lignocellulose, but the fungus-farming sub-family of higher termites has become similar in gut microbiota to the ancestral omnivorous cockroaches. To assess the importance of a fungus diet as a driver of community structure, we compare community compositions in the guts of experimentally manipulated Pycnoscelus surinamensis cockroaches fed on fungus cultivated by fungus-farming termites. MiSeq amplicon analysis of gut microbiotas from 49 gut samples showed a step-wise gradient pattern in community similarity that correlated with an increase in the proportion of fungal material provided to the cockroaches. Comparison of the taxonomic composition of manipulated communities to that of gut communities of a fungus-feeding termite species showed that although some bacteria OTUs shared by P. surinamensis and the farming termites increased in the guts of cockroaches on a fungal diet, cockroach communities remained distinct from those of termites. These results demonstrate that a fungal diet can play a role in structuring gut community composition, but at the same time exemplifies how original community compositions constrain the magnitude of such change.}, journal={PloS one}, year={2017}, month={Oct} }
@article{ikeda-ohtsubo_strassert_köhler_mikaelyan_gregor_mchardy_tringe_hugenholtz_radek_brune_2016, title={'Candidatus Adiutrix intracellularis', an endosymbiont of termite gut flagellates, is the first representative of a deep-branching clade of Deltaproteobacteria and a putative homoacetogen.}, volume={18}, url={http://europepmc.org/abstract/med/26914459}, DOI={10.1111/1462-2920.13234}, abstractNote={SummaryTermite gut flagellates are typically colonized by specific bacterial symbionts. Here we describe the phylogeny, ultrastructure and subcellular location of ‘Candidatus Adiutrix intracellularis’, an intracellular symbiont of Trichonympha collaris in the termite Zootermopsis nevadensis. It represents a novel, deep‐branching clade of uncultured Deltaproteobacteria widely distributed in intestinal tracts of termites and cockroaches. Fluorescence in situ hybridization and transmission electron microscopy localized the endosymbiont near hydrogenosomes in the posterior part and near the ectosymbiont ‘Candidatus Desulfovibrio trichonymphae’ in the anterior part of the host cell. The draft genome of ‘Ca. Adiutrix intracellularis’ obtained from a metagenomic library revealed the presence of a complete gene set encoding the Wood–Ljungdahl pathway, including two homologs of fdhF encoding hydrogenase‐linked formate dehydrogenases (FDHH) and all other components of the recently described hydrogen‐dependent carbon dioxide reductase (HDCR) complex, which substantiates previous claims that the symbiont is capable of reductive acetogenesis from CO2 and H2. The close phylogenetic relationship between the HDCR components and their homologs in homoacetogenic Firmicutes and Spirochaetes suggests that the deltaproteobacterium acquired the capacity for homoacetogenesis via lateral gene transfer. The presence of genes for nitrogen fixation and the biosynthesis of amino acids and cofactors indicate the nutritional nature of the symbiosis.}, number={8}, journal={Environmental microbiology}, author={Ikeda-Ohtsubo, W and Strassert, JF and Köhler, T and Mikaelyan, A and Gregor, I and McHardy, AC and Tringe, SG and Hugenholtz, P and Radek, R and Brune, A}, year={2016}, month={Sep}, pages={2548–2564,} }
@article{strassert_mikaelyan_woyke_brune_2016, title={Genome analysis of 'Candidatus Ancillula trichonymphae', first representative of a deep-branching clade of Bifidobacteriales, strengthens evidence for convergent evolution in flagellate endosymbionts.}, url={http://europepmc.org/abstract/med/27518440}, DOI={10.1111/1758-2229.12451}, abstractNote={SummaryThe flagellate protists in the hindgut of lower termites play an essential role in the digestion of lignocellulose. Most flagellate species are associated with host‐specific symbionts from various bacterial lineages, which typically lack cultured representatives. In this study, we analyzed the genome of ‘Candidatus Ancillula trichonymphae’, an endosymbiont of Trichonympha flagellates from dry‐wood termites, which represents a novel, family‐level lineage of uncultured Actinobacteria encountered so far only in termite guts. The draft genome of ‘Ca. A. trichonymphae’ (ca. 1.48 Mbp; 95% complete) revealed a purely fermentative metabolism that is probably fueled by xylose, N‐acetyl‐glucosamine and glycerol 3‐phosphate acquired from the flagellate host. The absence of fructose bisphosphate aldolase and the presence of a complete gene set encoding the phosphoketolase pathway underscore the sister position of the new lineage to Bifidobacteriaceae. The preservation of the pathways for the assimilation of ammonia and the synthesis of 18 amino acids and several cofactors and vitamins suggests that ‘Ca. A. trichonymphae’ – like other endosymbionts of termite gut flagellates – provides essential amino acids and vitamins to its host. Our findings corroborate the emerging concept that numerous lineages of unrelated flagellate endosymbionts have convergently evolved to fill similar ecological niches.}, journal={Environmental microbiology reports}, author={Strassert, JF and Mikaelyan, A and Woyke, T and Brune, A}, year={2016}, month={Aug} }
@article{microenvironmental heterogeneity of gut compartments drives bacterial community structure in wood- and humus-feeding higher termites._2016, url={https://doi.org/10.1093/femsec/fiw210}, DOI={10.1093/femsec/fiw210}, abstractNote={ABSTRACT Symbiotic digestion of lignocellulose in higher termites (family Termitidae) is accomplished by an exclusively prokaryotic gut microbiota. By deep sequencing of amplified 16S rRNA genes, we had identified diet as the primary determinant of bacterial community structure in a broad selection of termites specialized on lignocellulose in different stages of humification. Here, we increased the resolution of our approach to account for the pronounced heterogeneity in microenvironmental conditions and microbial activities in the major hindgut compartments. The community structure of consecutive gut compartments in each species strongly differed, but that of homologous compartments clearly converged, even among unrelated termites. While the alkaline P1 compartments of all termites investigated contained specific lineages of Clostridiales, the posterior hindgut compartments (P3, P4) differed between feeding groups and were predominantly colonized by putatively fiber‐associated lineages of Spirochaetes, Fibrobacteres and the TG3 phylum (wood and grass feeders) or diverse assemblages of Clostridiales and Bacteroidetes (humus and soil feeders). The results underscore that bacterial community structure in termite guts is driven by microenvironmental factors, such as pH, available substrates and gradients of O2 and H2, and inspire investigations on the functional roles of specific bacterial taxa in lignocellulose and humus digestion. &NA; Graphical Abstract Figure. Microenvironmental differences shape the distribution and abundance of bacterial populations in the gut compartments of higher termites.}, journal={FEMS microbiology ecology}, year={2016}, month={Oct} }
@article{li_dietrich_zhu_mikaelyan_ma_pi_liu_yang_brune_mo_2015, title={Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus.}, url={http://europepmc.org/abstract/med/26346907}, DOI={10.1111/1462-2920.13046}, abstractNote={SummaryFungus‐cultivating termites (Macrotermitinae) possess an elaborate strategy of lignocellulose digestion. It involves a lignocellulose‐degrading fungal symbiont (genus Termitomyces), a diverse gut microbiota and a characteristic labour division in food processing. In this study, using pyrotag sequencing and electron microscopy, we analysed the bacterial microbiota in the hindgut of Odontotermes formosanus and its fungus comb to investigate the spatial organization, establishment and temporal succession of the bacterial communities colonizing specific microhabitats. Our results document strong differences between the communities at the hindgut epithelium and the luminal fluid of newly moulted, young and old worker termites. The differences in community structure were consistent with the density, morphology and spatial distribution of bacterial cells and the pools of microbial metabolites in the hindgut compartment, underlining that both gut development and the age‐specific changes in diet affect the composition and functional role of their gut microbiota. These findings provide strong support for the concept that changes in diet and gut environment are important determinants of community structure because they create new niches for microbial symbionts.}, journal={Environmental microbiology}, author={Li, H and Dietrich, C and Zhu, N and Mikaelyan, A and Ma, B and Pi, R and Liu, Y and Yang, M and Brune, A and Mo, J}, year={2015}, month={Sep} }
@article{mikaelyan_köhler_lampert_rohland_boga_meuser_brune_2015, title={Classifying the bacterial gut microbiota of termites and cockroaches: A curated phylogenetic reference database (DictDb).}, volume={38}, url={http://europepmc.org/abstract/med/26283320}, DOI={10.1016/j.syapm.2015.07.004}, abstractNote={Recent developments in sequencing technology have given rise to a large number of studies that assess bacterial diversity and community structure in termite and cockroach guts based on large amplicon libraries of 16S rRNA genes. Although these studies have revealed important ecological and evolutionary patterns in the gut microbiota, classification of the short sequence reads is limited by the taxonomic depth and resolution of the reference databases used in the respective studies. Here, we present a curated reference database for accurate taxonomic analysis of the bacterial gut microbiota of dictyopteran insects. The Dictyopteran gut microbiota reference Database (DictDb) is based on the Silva database but was significantly expanded by the addition of clones from 11 mostly unexplored termite and cockroach groups, which increased the inventory of bacterial sequences from dictyopteran guts by 26%. The taxonomic depth and resolution of DictDb was significantly improved by a general revision of the taxonomic guide tree for all important lineages, including a detailed phylogenetic analysis of the Treponema and Alistipes complexes, the Fibrobacteres, and the TG3 phylum. The performance of this first documented version of DictDb (v. 3.0) using the revised taxonomic guide tree in the classification of short-read libraries obtained from termites and cockroaches was highly superior to that of the current Silva and RDP databases. DictDb uses an informative nomenclature that is consistent with the literature also for clades of uncultured bacteria and provides an invaluable tool for anyone exploring the gut community structure of termites and cockroaches.}, number={7}, journal={Systematic and applied microbiology}, author={Mikaelyan, A and Köhler, T and Lampert, N and Rohland, J and Boga, H and Meuser, K and Brune, A}, year={2015}, month={Oct}, pages={472–482} }
@article{mikaelyan_thompson_hofer_brune_2016, title={Deterministic Assembly of Complex Bacterial Communities in Guts of Germ-Free Cockroaches.}, volume={82}, url={http://europepmc.org/abstract/med/26655763}, DOI={10.1128/aem.03700-15}, abstractNote={ABSTRACT
The gut microbiota of termites plays important roles in the symbiotic digestion of lignocellulose. However, the factors shaping the microbial community structure remain poorly understood. Because termites cannot be raised under axenic conditions, we established the closely related cockroach
Shelfordella lateralis
as a germ-free model to study microbial community assembly and host-microbe interactions. In this study, we determined the composition of the bacterial assemblages in cockroaches inoculated with the gut microbiota of termites and mice using pyrosequencing analysis of their 16S rRNA genes. Although the composition of the xenobiotic communities was influenced by the lineages present in the foreign inocula, their structure resembled that of conventional cockroaches. Bacterial taxa abundant in conventional cockroaches but rare in the foreign inocula, such as
Dysgonomonas
and
Parabacteroides
spp., were selectively enriched in the xenobiotic communities. Donor-specific taxa, such as endomicrobia or spirochete lineages restricted to the gut microbiota of termites, however, either were unable to colonize germ-free cockroaches or formed only small populations. The exposure of xenobiotic cockroaches to conventional adults restored their normal microbiota, which indicated that autochthonous lineages outcompete foreign ones. Our results provide experimental proof that the assembly of a complex gut microbiota in insects is deterministic.
}, number={4}, journal={Applied and environmental microbiology}, author={Mikaelyan, A and Thompson, CL and Hofer, MJ and Brune, A}, year={2016}, month={Feb}, pages={1256–1263,} }
@article{mikaelyan_dietrich_köhler_poulsen_sillam-dussès_brune_2015, title={Diet is the primary determinant of bacterial community structure in the guts of higher termites.}, volume={24}, url={http://europepmc.org/abstract/med/26348261}, DOI={10.1111/mec.13376}, abstractNote={AbstractThe gut microbiota of termites plays critical roles in the symbiotic digestion of lignocellulose. While phylogenetically ‘lower termites’ are characterized by a unique association with cellulolytic flagellates, higher termites (family Termitidae) harbour exclusively prokaryotic communities in their dilated hindguts. Unlike the more primitive termite families, which primarily feed on wood, they have adapted to a variety of lignocellulosic food sources in different stages of humification, ranging from sound wood to soil organic matter. In this study, we comparatively analysed representatives of different taxonomic lineages and feeding groups of higher termites to identify the major drivers of bacterial community structure in the termite gut, using amplicon libraries of 16S rRNA genes from 18 species of higher termites. In all analyses, the wood‐feeding species were clearly separated from humus and soil feeders, irrespective of their taxonomic affiliation, offering compelling evidence that diet is the primary determinant of bacterial community structure. Within each diet group, however, gut communities of termites from the same subfamily were more similar than those of distantly related species. A highly resolved classification using a curated reference database revealed only few genus‐level taxa whose distribution patterns indicated specificity for certain host lineages, limiting any possible cospeciation between the gut microbiota and host to short evolutionary timescales. Rather, the observed patterns in the host‐specific distribution of the bacterial lineages in termite guts are best explained by diet‐related differences in the availability of microhabitats and functional niches.}, number={20}, journal={Molecular ecology}, author={Mikaelyan, A and Dietrich, C and Köhler, T and Poulsen, M and Sillam-Dussès, D and Brune, A}, year={2015}, month={Oct}, pages={5284–5295} }
@article{rossmassler_dietrich_thompson_mikaelyan_nonoh_scheffrahn_sillam-dussès_brune_2015, title={Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites.}, volume={3}, url={http://europepmc.org/abstract/med/26607965}, DOI={10.1186/s40168-015-0118-1}, abstractNote={Termites are important contributors to carbon and nitrogen cycling in tropical ecosystems. Higher termites digest lignocellulose in various stages of humification with the help of an entirely prokaryotic microbiota housed in their compartmented intestinal tract. Previous studies revealed fundamental differences in community structure between compartments, but the functional roles of individual lineages in symbiotic digestion are mostly unknown. Here, we conducted a highly resolved analysis of the gut microbiota in six species of higher termites that feed on plant material at different levels of humification. Combining amplicon sequencing and metagenomics, we assessed similarities in community structure and functional potential between the major hindgut compartments (P1, P3, and P4). Cluster analysis of the relative abundances of orthologous gene clusters (COGs) revealed high similarities among wood- and litter-feeding termites and strong differences to humivorous species. However, abundance estimates of bacterial phyla based on 16S rRNA genes greatly differed from those based on protein-coding genes. Community structure and functional potential of the microbiota in individual gut compartments are clearly driven by the digestive strategy of the host. The metagenomics libraries obtained in this study provide the basis for future studies that elucidate the fundamental differences in the symbiont-mediated breakdown of lignocellulose and humus by termites of different feeding groups. The high proportion of uncultured bacterial lineages in all samples calls for a reference-independent approach for the correct taxonomic assignment of protein-coding genes.}, author={Rossmassler, K and Dietrich, C and Thompson, C and Mikaelyan, A and Nonoh, JO and Scheffrahn, RH and Sillam-Dussès, D and Brune, A}, year={2015}, pages={56,} }
@article{analysis of midgut bacterial community structure of neanthes chilkaensis from polluted mudflats of gorai, mumbai, india_2014, DOI={10.4236/aim.2014.413101}, abstractNote={Adaptation of microbial communities to anthropogenic stress has often been shown to involve reduction in diversity and in selective enrichment of species capable of survival. The gut bacterial community of pollution-stressed polychaete Neanthes chilkaensis was studied using cultivation dependent and independent approaches. The possible role of the gut bacteria in remediation of pollutants was also studied. The analysis of clones covering about 90% of the 16S rRNA clone library indicated that the majority of the taxa in the library resemble GenBank entries of aromatic- hydrocarbon pollutant degraders. Among them Firmicutes and Actinobacteria were dominant. About 84% of the gut isolates were capable of utilizing PAHs as sole carbon sources while 20% of isolates were found to produce biosurfactants. Production of surfactant along with capability to utilize PAH and other pollutants indicate the role of the gut community in alleviating the pollution stress. The results also show the potential source of microorganisms with industrial and environmental application.}, year={2014}, month={Oct} }
@article{otani_mikaelyan_nobre_hansen_koné_sørensen_aanen_boomsma_brune_poulsen_2014, title={Identifying the core microbial community in the gut of fungus-growing termites.}, volume={23}, url={http://europepmc.org/abstract/med/25066007}, DOI={10.1111/mec.12874}, abstractNote={AbstractGut microbes play a crucial role in decomposing lignocellulose to fuel termite societies, with protists in the lower termites and prokaryotes in the higher termites providing these services. However, a single basal subfamily of the higher termites, the Macrotermitinae, also domesticated a plant biomass‐degrading fungus (Termitomyces), and how this symbiont acquisition has affected the fungus‐growing termite gut microbiota has remained unclear. The objective of our study was to compare the intestinal bacterial communities of five genera (nine species) of fungus‐growing termites to establish whether or not an ancestral core microbiota has been maintained and characterizes extant lineages. Using 454‐pyrosequencing of the 16S rRNA gene, we show that gut communities have representatives of 26 bacterial phyla and are dominated by Firmicutes, Bacteroidetes, Spirochaetes, Proteobacteria and Synergistetes. A set of 42 genus‐level taxa was present in all termite species and accounted for 56–68% of the species‐specific reads. Gut communities of termites from the same genus were more similar than distantly related species, suggesting that phylogenetic ancestry matters, possibly in connection with specific termite genus‐level ecological niches. Finally, we show that gut communities of fungus‐growing termites are similar to cockroaches, both at the bacterial phylum level and in a comparison of the core Macrotermitinae taxa abundances with representative cockroach, lower termite and higher nonfungus‐growing termites. These results suggest that the obligate association with Termitomyces has forced the bacterial gut communities of the fungus‐growing termites towards a relatively uniform composition with higher similarity to their omnivorous relatives than to more closely related termites.}, number={18}, journal={Molecular ecology}, author={Otani, S and Mikaelyan, A and Nobre, T and Hansen, LH and Koné, NA and Sørensen, SJ and Aanen, DK and Boomsma, JJ and Brune, A and Poulsen, M}, year={2014}, month={Sep}, pages={4631–4644} }
@article{bauer_lampert_mikaelyan_köhler_maekawa_brune_2015, title={Physicochemical conditions, metabolites and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae).}, volume={91}, url={http://europepmc.org/abstract/med/25764554}, DOI={10.1093/femsec/fiu028}, abstractNote={While the gut microbiota of termites and its role in symbiotic digestion have been studied for decades, little is known about the bacteria colonizing the intestinal tract of the distantly related wood-feeding cockroaches (Blaberidae: Panesthiinae). Here, we show that physicochemical gut conditions and microbial fermentation products in the gut of Panesthia angustipennis resemble that of other cockroaches. Microsensor measurements confirmed that all gut compartments were anoxic at the center and had a slightly acidic to neutral pH and a negative redox potential. While acetate dominated in all compartments, lactate and hydrogen accumulated only in the crop. The high, hydrogen-limited rates of methane emission from living cockroaches were in agreement with the restriction of F420-fluorescent methanogens to the hindgut. The gut microbiota of both P. angustipennis and Salganea esakii differed strongly between compartments, with the highest density and diversity in the hindgut, but similarities between homologous compartments of both cockroaches indicated a specificity of the microbiota for their respective habitats. While some lineages were most closely related to the gut microbiota of omnivorous cockroaches and wood- or litter-feeding termites, others have been encountered also in vertebrates, reinforcing the hypothesis that strong environmental selection drives community structure in the cockroach gut.}, number={2}, journal={FEMS microbiology ecology}, author={Bauer, E and Lampert, N and Mikaelyan, A and Köhler, T and Maekawa, K and Brune, A}, year={2015}, month={Feb}, pages={1–14} }
@article{the fibre-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (nasutitermes spp.)_2014, DOI={10.1111/1462-2920.12425}, abstractNote={SummaryTermites digest lignocellulose with the help of their symbiotic gut microbiota. In the hindgut of evolutionary lower termites, a dense community of cellulolytic flagellates sequesters wood particles from the hindgut content into their digestive vacuoles. In higher termites (family Termitidae), which possess an entirely prokaryotic microbiota, the wood particles are available for bacterial colonization. Substantial particle‐associated cellulase activities have been detected in the hindgut of Nasutitermes species, but the microorganisms responsible for these activities and their potential association with the wood fibres remain to be studied. Here, we used density‐gradient centrifugation to separate wood fibres and adherent bacterial cells from cells freely suspended in the hindgut fluid. In Nasutitermes corniger, the fibre fraction contained 28% of the DNA and 45% of the cellulase activity in the luminal contents (P3 region). Community fingerprinting (terminal restriction fragment length polymorphism) and pyrotag sequencing analysis of the bacterial 16S rRNA genes demonstrated that the wood fibres in the hindgut of both N. corniger and N. takasagoensis are specifically colonized by members of Fibrobacteres, the TG3 phylum, and certain lineages of Spirochaetes characteristic of the gut microbiota of wood‐feeding higher termites. We propose that the loss of flagellates in higher termites provided a new niche for fibre‐associated cellulolytic bacteria.}, journal={Environmental Microbiology}, year={2014}, month={Jan} }
@article{thompson_vier_mikaelyan_wienemann_brune_2012, title={'Candidatus Arthromitus' revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae.}, volume={14}, url={http://europepmc.org/abstract/med/22436008}, DOI={10.1111/j.1462-2920.2012.02731.x}, abstractNote={SummaryThe name Arthromitus has been applied collectively to conspicuous filamentous bacteria found in the hindguts of termites and other arthropods. First observed by Joseph Leidy in 1849, the identity of these filaments has remained contentious. While Margulis and colleagues declared them to be a life stage of Bacillus cereus, others have assumed them to belong to the same lineage as the segmented filamentous bacteria (SFB) from vertebrate guts, a group that has garnered much attention due to their unique ability to specifically modulate their host's immune response. Both SFB and Arthromitus filaments from arthropod guts were grouped under provisional name ‘Candidatus Arthromitus’ by Snel and colleagues as they share a striking similarity in terms of their morphology and close contact to the host gut wall. While SFB form a distinct lineage within the family Clostridiaceae, the identity of the filaments from arthropod guts remains elusive. Using whole‐genome amplification of single filaments capillary picked from termite guts and fluorescence in situ hybridization of 16S rRNA with group‐specific oligonucleotide probes, we show that they represent a monophyletic lineage within the family Lachnospiraceae distinct from that of SFB. Therefore, ‘Candidatus Arthromitus’ can no longer be used for both groups. Given the historic precedence, we propose to reserve this name for the filaments that were originally described by Leidy. For the SFB from vertebrate guts, we propose the provisional name ‘Candidatus Savagella’ in honour of the American gut microbiologist Dwayne C. Savage, who was the first to describe that important bacterial group.}, number={6}, journal={Environmental microbiology}, author={Thompson, CL and Vier, R and Mikaelyan, A and Wienemann, T and Brune, A}, year={2012}, month={Jun}, pages={1454–1465} }
@article{thompson_mikaelyan_brune_2013, title={Immune-modulating gut symbionts are not "Candidatus Arthromitus".}, volume={6}, url={http://europepmc.org/abstract/med/23013646}, DOI={10.1038/mi.2012.91}, abstractNote={To the Editor: It is becoming increasingly evident that the microbial community of the intestine is critical for refining the immune system of its host. Nothing illustrates this better than the segmented filamentous bacteria (SFB). These vertebrate gut symbionts are tightly anchored to epithelial cells of the ileal mucosa and possess the unique ability to specifically modulate the host immune response, which has consequences that extend beyond the gut wall. SFB trigger a diverse array of immune functions, inducing innate immune responses,1Keilbaugh SA Activation of RegIIIβ/γ and interferon γ expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut.Gut. 2005; 54,: 623-62910.1136/gut.2004.056028Crossref PubMed Scopus (70) Google Scholar, 2Gaboriau-Routhiau V The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses.Immunity. 2009; 31,: 677-68910.1016/j.immuni.2009.08.020Abstract Full Text Full Text PDF PubMed Scopus (1069) Google Scholar, 3Ivanov II Induction of intestinal Th17 cells by segmented filamentous bacteria.Cell. 2009; 139,: 485-49810.1016/j.cell.2009.09.033Abstract Full Text Full Text PDF PubMed Scopus (3169) Google Scholar increasing and activating cytotoxic intraepithelial lymphocyte populations,4Umesaki Y Okada Y Matsumoto S Imaoka A Setoyama H Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse.Microbiol. Immunol. 1995; 39,: 555-56210.1111/j.1348-0421.1995.tb02242.xCrossref PubMed Scopus (275) Google Scholar and coordinating T-cell responses, including the specific induction of CD4+ T-helper 17 cells.2Gaboriau-Routhiau V The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses.Immunity. 2009; 31,: 677-68910.1016/j.immuni.2009.08.020Abstract Full Text Full Text PDF PubMed Scopus (1069) Google Scholar, 3Ivanov II Induction of intestinal Th17 cells by segmented filamentous bacteria.Cell. 2009; 139,: 485-49810.1016/j.cell.2009.09.033Abstract Full Text Full Text PDF PubMed Scopus (3169) Google Scholar They appear to act as a double-edged sword for the mammalian immune system—on one side mediating protective immunity by potently inducing IgA-secreting cells5Talham GL Jiang HQ Bos NA Cebra JJ Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system.Infect. Immun. 1999; 67,: 1992-2000Crossref PubMed Google Scholar but on the other side promoting autoimmune disorders by triggering rheumatoid arthritis6Wu H-S Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells.Immunity. 2010; 32,: 815-82710.1016/j.immuni.2010.06.001Abstract Full Text Full Text PDF PubMed Scopus (1168) Google Scholar and multiple sclerosis7Lee YK Menezes JS Umesaki Y Mazmanian SK Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis.Proc. Natl Acad. Sci. USA. 2011; 108,: 4615-462210.1073/pnas.1000082107Crossref PubMed Scopus (943) Google Scholar in experimental mouse models. This makes SFB one of the very few examples of gut commensals that can stimulate the postnatal maturation of the immune system. Although the study of gut bacteria has traditionally occurred within the realm of microbiology, immunological studies have formed the vanguard in the quest to understand the SFB. This is why we wish to draw attention to proposed changes to the classification of this immunologically significant group. When Snel et al.8Snel J Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of “Candidatus Arthromitus”.Int. J. Syst. Bacteriol. 1995; 45,: 780-78210.1099/00207713-45-4-780Crossref PubMed Scopus (129) Google Scholar showed that SFB form a distinct lineage of uncultivated bacteria within the bacterial family Clostridiaceae, they assigned them to the genus Arthromitus—a group of equally conspicuous bacterial filaments from arthropod guts that had been described by the American scientist Joseph Leidy over 160 years ago.9Leidy J On the existence of entophyta in healthy animals, as a natural condition.Proc. Acad. Natl Sci. Phila. 1849; 4,: 225-233Google Scholar However, assuming relatedness based on morphology alone was a mistake. Using molecular phylogenetic analysis of 16S rRNA gene sequences, we have recently shown that Leidy’s Arthromitus in fact belongs to a different bacterial family, the Lachnospiraceae10Thompson CL Vier R Mikaelyan A Wienemann T Brune A ‘Candidatus Arthromitus' revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae.Environ. Microbiol. 2012; 14,: 1454-146510.1111/j.1462-2920.2012.02731.xCrossref PubMed Scopus (74) Google Scholar—despite their striking similarity to mammalian SFB (Figure 1). Given the immunological importance of mammalian SFB, it is imperative that these two bacterial groups be distinguished from each other. Biological functions attributed to Leidy’s Arthromitus will not necessarily apply to mammalian SFB and vice versa. In view of their distinct phylogenetic positions, the same name can no longer be used for both groups. Given the historical priority of Leidy’s Arthromitus, and the apparent absence of SFB-like 16S rRNA gene sequences from arthropod guts, we proposed to rename SFB to “Candidatus Savagella”10Thompson CL Vier R Mikaelyan A Wienemann T Brune A ‘Candidatus Arthromitus' revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae.Environ. Microbiol. 2012; 14,: 1454-146510.1111/j.1462-2920.2012.02731.xCrossref PubMed Scopus (74) Google Scholar—in honor of the American gut microbiologist Dwayne C. Savage, who was the first to describe this bacterial group in the ileum of rodents.11Davis CP Savage DC Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract.Infect. Immun. 1974; 10,: 948-956Crossref PubMed Scopus (0) Google Scholar Download .ppt (1.04 MB) Help with ppt files PowerPoint slide for Fig. 1 The authors declared no conflict of interest.}, number={1}, journal={Mucosal immunology}, author={Thompson, CL and Mikaelyan, A and Brune, A}, year={2013}, month={Jan}, pages={200–201} }