Inter-species microbiota transplantation recapitulates microbial acquisition and persistence in mosquitoes

AbstractBackgroundMosquitoes harbor microbial communities that play important roles in their growth, survival, reproduction, and ability to transmit human pathogens. Microbiome transplantation approaches are often used to study host-microbe interactions and identify microbial taxa and assemblages associated with health or disease. However, no such approaches have been developed to manipulate the microbiota of mosquitoes.ResultsHere, we developed an approach to transfer entire microbial communities between mosquito cohorts. We undertook transfers between (Culex quinquefasciatus to Aedes aegypti) and within (Ae. aegypti to Ae. aegypti) species to validate the approach and determine the number of mosquitoes required to prepare donor microbiota. After the transfer, we monitored mosquito development and microbiota dynamics throughout the life cycle. Typical holometabolous lifestyle-related microbiota structures were observed, with higher dynamics of microbial structures in larval stages, including the larval water, and less diversity in adults. Microbiota diversity in recipient adults was also more similar to the microbiota diversity in donor adults.ConclusionsThis study provides the first evidence for successful microbiome transplantation in mosquitoes. Our results highlight the value of such methods for studying mosquito-microbe interactions and lay the foundation for future studies to elucidate the factors underlying microbiota acquisition, assembly, and function in mosquitoes under controlled conditions.

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Parallel changes in gut microbiome composition and function in parallel local adaptation and speciation

10.1101/736843 ◽

2019 ◽

Cited By ~ 2

Author(s):

Diana J. Rennison ◽

Seth M. Rudman ◽

Dolph Schluter

Keyword(s):

Microbial Communities ◽

Local Adaptation ◽

Biotic Interactions ◽

Ecological Speciation ◽

Microbiome Composition ◽

Interacting Species ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

And Function ◽

Host Evolution

AbstractThe processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet, relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we utilize three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification.

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Microbiota as Therapeutic Targets

Digestive Diseases ◽

10.1159/000445263 ◽

2016 ◽

Vol 34 (5) ◽

pp. 558-565 ◽

Cited By ~ 10

Author(s):

Ramnik J. Xavier

Keyword(s):

Gastrointestinal Tract ◽

Microbial Communities ◽

Association Studies ◽

Microbial Community Composition ◽

Great Promise ◽

Host Immune System ◽

Genome Wide Association Studies ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

And Function

Background: Inflammatory bowel disease (IBD) represents a family of diseases including Crohn's disease and ulcerative colitis. IBD has garnered significant attention in recent years due to successes in 2 areas of basic science: complex human genetics and host-microbe interactions. Advances in understanding the genetics of IBD, mainly driven by genome-wide association studies, have identified more than 160 genetic loci that modulate the risk of disease. Notably, several of these genes have pointed to alterations in host-microbe interactions as being critical factors in pathogenesis. Investigations into the microbial communities of the gastrointestinal tract (or the ‘gut microbiome') in IBD have yielded important insights into several aspects of interactions between microbiota and the host immune system, including how alterations to microbial community composition and function have important consequences for immune homeostasis. Key Messages: The anatomy of the gastrointestinal tract plays a role in defining not only intestinal function, but also the microbial ecosystem that lives within the gut. Careful investigations into the composition and function of these microbial communities have suggested that patients with IBD have an imbalance in their gut microbiota, termed dysbiosis. These studies, as well as studies using samples from healthy individuals, have begun to uncover mechanisms of crosstalk between particular microbes (and microbial products) and immunomodulatory pathways, alterations which may drive immune diseases such as IBD. Conclusions: Investigations into the role of the microbiome in IBD have provided important clues to potential pathogenic mechanisms. Harnessing this knowledge to develop therapeutics and identify biomarkers is currently a major translational goal, holding great promise for clinically meaningful progress.

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Parallel changes in gut microbiome composition and function during colonization, local adaptation and ecological speciation

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.1911 ◽

2019 ◽

Vol 286 (1916) ◽

pp. 20191911 ◽

Cited By ~ 7

Author(s):

Diana J. Rennison ◽

Seth M. Rudman ◽

Dolph Schluter

Keyword(s):

Microbial Communities ◽

Local Adaptation ◽

Biotic Interactions ◽

Ecological Speciation ◽

Microbiome Composition ◽

Interacting Species ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

And Function ◽

Host Evolution

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from the repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we use three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host–microbe interactions might play an important role in host adaptation and diversification.

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Neurons interact with the microbiome: an evolutionary-informed perspective

Neuroforum ◽

10.1515/nf-2021-0003 ◽

2021 ◽

Vol 0 (0) ◽

Author(s):

Christoph Giez ◽

Alexander Klimovich ◽

Thomas C. G. Bosch

Keyword(s):

Nervous System ◽

Neural Circuits ◽

Current Knowledge ◽

System Development ◽

Nervous System Development ◽

Comprehensive Understanding ◽

Strategic Model ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

And Function

Abstract Animals have evolved within the framework of microbes and are constantly exposed to diverse microbiota. Microbes colonize most, if not all, animal epithelia and influence the activity of many organs, including the nervous system. Therefore, any consideration on nervous system development and function in the absence of the recognition of microbes will be incomplete. Here, we review the current knowledge on the nervous systems of Hydra and its role in the host–microbiome communication. We show that recent advances in molecular and imaging methods are allowing a comprehensive understanding of the capacity of such a seemingly simple nervous system in the context of the metaorganism. We propose that the development, function and evolution of neural circuits must be considered in the context of host–microbe interactions and present Hydra as a strategic model system with great basic and translational relevance for neuroscience.

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A Microbial Perspective on the Grand Challenges in Comparative Animal Physiology

mSystems ◽

10.1128/msystems.00146-17 ◽

2018 ◽

Vol 3 (2) ◽

Cited By ~ 4

Author(s):

Kevin D. Kohl

Keyword(s):

Microbial Communities ◽

Vertical Integration ◽

Temporal Integration ◽

Data Sets ◽

Grand Challenges ◽

Animal Physiology ◽

Physiological Processes ◽

Microbe Interactions ◽

Animal Hosts ◽

Host Microbe Interactions

ABSTRACTInteractions with microbial communities can have profound influences on animal physiology, thereby impacting animal performance and fitness. Therefore, it is important to understand the diversity and nature of host-microbe interactions in various animal groups (invertebrates, fish, amphibians, reptiles, birds, and mammals). In this perspective, I discuss how the field of host-microbe interactions can be used to address topics that have been identified as grand challenges in comparative animal physiology: (i) horizontal integration of physiological processes across organisms, (ii) vertical integration of physiological processes across organizational levels within organisms, and (iii) temporal integration of physiological processes during evolutionary change. Addressing these challenges will require the use of a variety of animal models and the development of systems approaches that can integrate large, multiomic data sets from both microbial communities and animal hosts. Integrating host-microbe interactions into the established field of comparative physiology represents an exciting frontier for both fields.

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Optimal integration between host physiology and functions of the gut microbiome

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0594 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190594 ◽

Cited By ~ 4

Author(s):

Samantha S. Fontaine ◽

Kevin D. Kohl

Keyword(s):

Microbial Communities ◽

Physiological Function ◽

Biological Organization ◽

Theme Issue ◽

Microbe Interactions ◽

Host Physiology ◽

Host Microbe Interactions ◽

Host Evolution ◽

Physiological Systems

Host-associated microbial communities have profound impacts on animal physiological function, especially nutrition and metabolism. The hypothesis of ‘symmorphosis’, which posits that the physiological systems of animals are regulated precisely to meet, but not exceed, their imposed functional demands, has been used to understand the integration of physiological systems across levels of biological organization. Although this idea has been criticized, it is recognized as having important heuristic value, even as a null hypothesis, and may, therefore, be a useful tool in understanding how hosts evolve in response to the function of their microbiota. Here, through a hologenomic lens, we discuss how the idea of symmorphosis may be applied to host-microbe interactions. Specifically, we consider scenarios in which host physiology may have evolved to collaborate with the microbiota to perform important functions, and, on the other hand, situations in which services have been completely outsourced to the microbiota, resulting in relaxed selection on host pathways. Following this theoretical discussion, we finally suggest strategies by which these currently speculative ideas may be explicitly tested to further our understanding of host evolution in response to their associated microbial communities. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Inferring directional relationships in microbial communities using signed Bayesian networks

BMC Genomics ◽

10.1186/s12864-020-07065-0 ◽

2020 ◽

Vol 21 (S6) ◽

Author(s):

Musfiqur Sazal ◽

Kalai Mathee ◽

Daniel Ruiz-Perez ◽

Trevor Cickovski ◽

Giri Narasimhan

Keyword(s):

Microbial Community ◽

Bayesian Networks ◽

Bayesian Network ◽

Microbial Communities ◽

Community Analysis ◽

Vital Role ◽

Microbe Interactions ◽

Health And Disease ◽

Colonization Patterns ◽

Host Microbe Interactions

Abstract Background Microbe-microbe and host-microbe interactions in a microbiome play a vital role in both health and disease. However, the structure of the microbial community and the colonization patterns are highly complex to infer even under controlled wet laboratory conditions. In this study, we investigate what information, if any, can be provided by a Bayesian Network (BN) about a microbial community. Unlike the previously proposed Co-occurrence Networks (CoNs), BNs are based on conditional dependencies and can help in revealing complex associations. Results In this paper, we propose a way of combining a BN and a CoN to construct a signed Bayesian Network (sBN). We report a surprising association between directed edges in signed BNs and known colonization orders. Conclusions BNs are powerful tools for community analysis and extracting influences and colonization patterns, even though the analysis only uses an abundance matrix with no temporal information. We conclude that directed edges in sBNs when combined with negative correlations are consistent with and strongly suggestive of colonization order.

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Host-Microbe Interactions in Caenorhabditis elegans

ISRN Microbiology ◽

10.1155/2013/356451 ◽

2013 ◽

Vol 2013 ◽

pp. 1-7 ◽

Cited By ~ 30

Author(s):

Rui Zhang ◽

Aixin Hou

Keyword(s):

Life Cycle ◽

Microbial Pathogens ◽

Model Organisms ◽

Short Life ◽

C Elegans ◽

Complex Microbial Community ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

Laboratory Maintenance ◽

Genetic Mutants

A good understanding of how microbes interact with hosts has a direct bearing on our capability of fighting infectious microbial pathogens and making good use of beneficial ones. Among the model organisms used to study reciprocal actions among microbes and hosts, C. elegans may be the most advantageous in the context of its unique attributes such as the short life cycle, easiness of laboratory maintenance, and the availability of different genetic mutants. This review summarizes the recent advances in understanding host-microbe interactions in C. elegans. Although these investigations have greatly enhanced our understanding of C. elegans-microbe relationships, all but one of them involve only one or few microbial species. We argue here that more research is needed for exploring the evolution and establishment of a complex microbial community in the worm’s intestine and its interaction with the host.

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Candidate pathogenicity islands in the genome of ‘CandidatusRickettsiella isopodorum’, an intracellular bacterium infecting terrestrial isopod crustaceans

PeerJ ◽

10.7717/peerj.2806 ◽

2016 ◽

Vol 4 ◽

pp. e2806 ◽

Cited By ~ 9

Author(s):

YaDong Wang ◽

Christopher Chandler

Keyword(s):

Genomic Island ◽

Genomic Sequence ◽

Genomic Analysis ◽

Comparative Genomic Analysis ◽

Comparative Genomic ◽

Photorhabdus Luminescens ◽

Future Studies ◽

Terrestrial Isopod ◽

Microbe Interactions ◽

Host Microbe Interactions

The bacterial genusRickettsiellabelongs to the order Legionellales in the Gammaproteobacteria, and consists of several described species and pathotypes, most of which are considered to be intracellular pathogens infecting arthropods. Two members of this genus,R. grylliandR. isopodorum, are known to infect terrestrial isopod crustaceans. In this study, we assembled a draft genomic sequence forR. isopodorum, and performed a comparative genomic analysis withR. grylli. We found evidence for several candidate genomic island regions inR. isopodorum, none of which appear in the previously availableR. grylligenome sequence.Furthermore, one of these genomic island candidates inR. isopodorumcontained a gene that encodes a cytotoxin partially homologous to those found inPhotorhabdus luminescensandXenorhabdus nematophilus(Enterobacteriaceae), suggesting that horizontal gene transfer may have played a role in the evolution of pathogenicity inRickettsiella. These results lay the groundwork for future studies on the mechanisms underlying pathogenesis inR. isopodorum, and this system may provide a good model for studying the evolution of host-microbe interactions in nature.

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Inferring directional relationships in microbial communities using signed Bayesian networks

10.1101/2020.02.18.955344 ◽

2020 ◽

Cited By ~ 1

Author(s):

Musfiqur Sazal ◽

Kalai Mathee ◽

Daniel Ruiz-Perez ◽

Trevor Cickovski ◽

Giri Narasimhan

Keyword(s):

Microbial Community ◽

Bayesian Networks ◽

Bayesian Network ◽

Microbial Communities ◽

Community Analysis ◽

Vital Role ◽

Microbe Interactions ◽

Health And Disease ◽

Colonization Patterns ◽

Host Microbe Interactions

AbstractBackgroundMicrobe-microbe and host-microbe interactions in a microbiome play a vital role in both health and disease. However, the structure of the microbial community and the colonization patterns are highly complex to infer even under controlled wet laboratory conditions. In this study, we investigate what information, if any, can be provided by a Bayesian Network (BN) about a microbial community. Unlike the previously proposed Co-occurrence Networks (CoNs), BNs are based on conditional dependencies and can help in revealing complex associations.ResultsIn this paper, we propose a way of combining a BN and a CoN to construct a signed Bayesian Network (sBN). We report a surprising association between directed edges in signed BNs and known colonization orders.ConclusionsBNs are powerful tools for community analysis and extracting influences and colonization patterns, even though the analysis only uses an abundance matrix with no temporal information. We conclude that directed edges in sBNs when combined with negative correlations are consistent with and strongly suggestive of colonization order.

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