Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

Brune, Andreas

doi:10.1111/mec.13688

Cited by 4 publications

(3 citation statements)

References 14 publications

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“…We also found a number of bacterial lineages that had a more general affinity for animal guts, such as members of the Clostridiales family Ruminococcaceae, which made up 16.5% of the reads that we analyzed and are considered to contribute to cellulose and hemicellulose digestion in their intestinal habitats [34,35]. Our results provide support for the theory of ecological fitting [36], which posits that traits developed by a symbiont during its evolutionary history may be co-opted for a new purpose in a different host. We predict that some groups of bacteria present in termites might be much more widespread among the guts of other organisms than currently appreciated.…”

Section: Resultssupporting

confidence: 72%

Rampant Host Switching Shaped the Termite Gut Microbiome

et al. 2018

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The gut microbiota of animals exert major effects on host biology [1]. Although horizontal transfer is generally considered the prevalent route for the acquisition of gut bacteria in mammals [2], some bacterial lineages have co-speciated with their hosts on timescales of several million years [3]. Termites harbor a complex gut microbiota, and their advanced social behavior provides the potential for long-term vertical symbiont transmission, and co-evolution of gut symbionts and host [4-6]. Despite clear evolutionary patterns in the gut microbiota of termites [7], a consensus on how microbial communities were assembled during termite diversification has yet to be reached. Although some studies have concluded that vertical transmission has played a major role [8, 9], others indicate that diet and gut microenvironment have been the primary determinants shaping microbial communities in termite guts [7, 10]. To address this issue, we examined the gut microbiota of 94 termite species, through 16S rRNA metabarcoding. We analyzed the phylogeny of 211 bacterial lineages obtained from termite guts, including their closest relatives from other environments, which were identified using BLAST. The results provided strong evidence for rampant horizontal transfer of gut bacteria between termite host lineages. Although the majority of termite-derived phylotypes formed large monophyletic groups, indicating high levels of niche specialization, numerous other clades were interspersed with bacterial lineages from the guts of other animals. Our results indicate that "mixed-mode" transmission, which combines colony-to-offspring vertical transmission with horizontal colony-to-colony transfer, has been the primary driving force shaping the gut microbiota of termites.

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Section: Resultssupporting

confidence: 72%

Rampant Host Switching Shaped the Termite Gut Microbiome

et al. 2018

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“…Insects have evolved elaborate mechanisms to do so, including transovarial infection, egg smearing or delivery of symbionts in capsules, or jelly-like secretions ( Douglas, 1989 ; Kikuchi, 2009 ; Salem et al, 2015 ). Nonetheless, many animals and plants acquire their symbionts via horizontal transmission from the environment ( Kikuchi et al, 2007 ; Brune, 2016 ; Hartmann et al, 2017 ) or through mixed-mode transmission, a combination of both vertical and horizontal mechanisms ( Ebert, 2013 ). Importantly, strict vertical transmission and increasing dependence are usually associated with severe genomic consequences for bacterial symbionts.…”

Section: Introductionmentioning

confidence: 99%

Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment

et al. 2021

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Many phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction between microbe, insect, and plant. Here, we focus on two bacterial symbionts of the darkling beetle Lagria villosa that belong to the genus Burkholderia; the culturable strain B. gladioli Lv-StA and the reduced-genome strain Burkholderia Lv-StB. The strains can be transmitted vertically and confer protection to the beetle’s eggs, but Lv-StA can also proliferate in plants, and both symbiont strains have presumably evolved from plant pathogens. Notably, little is known about the role of the environment for the transmission dynamics and the maintenance of the symbionts. Through manipulative assays, we demonstrate the transfer of the symbionts from the beetle to wheat, rice and soybean plants, as well as leaf litter. In addition, we confirm that aposymbiotic larvae can pick up Lv-StA from dry leaves and the symbiont can successfully establish in the beetle’s symbiotic organs. Also, we show that the presence of plants and soil in the environment improves symbiont maintenance. These results indicate that the symbionts of L. villosa beetles are still capable of interacting with plants despite signatures of genome erosion and suggest that a mixed-mode of bacterial transmission is likely key for the persistence of the symbiosis.

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“…This further indicates that soil animals are important as repositories of microbial biodiversity. The existence of this microbial niche was largely unknown prior to the present study and raises the issue that the holobiont of soil fauna should be considered as a target of conservation [ 62 , 63 ].…”

Section: Discussionmentioning

confidence: 99%

Trophic level drives the host microbiome of soil invertebrates at a continental scale

et al. 2021

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Background Increasing our knowledge of soil biodiversity is fundamental to forecast changes in ecosystem functions under global change scenarios. All multicellular organisms are now known to be holobionts, containing large assemblages of microbial species. Soil fauna is now known to have thousands of species living within them. However, we know very little about the identity and function of host microbiome in contrasting soil faunal groups, across different terrestrial biomes, or at a large spatial scale. Here, we examined the microbiomes of multiple functionally important soil fauna in contrasting terrestrial ecosystems across China. Results Different soil fauna had diverse and unique microbiomes, which were also distinct from those in surrounding soils. These unique microbiomes were maintained within taxa across diverse sampling sites and in contrasting terrestrial ecosystems. The microbiomes of nematodes, potworms, and earthworms were more difficult to predict using environmental data, compared to those of collembolans, oribatid mites, and predatory mites. Although stochastic processes were important, deterministic processes, such as host selection, also contributed to the assembly of unique microbiota in each taxon of soil fauna. Microbial biodiversity, unique microbial taxa, and microbial dark matter (defined as unidentified microbial taxa) all increased with trophic levels within the soil food web. Conclusions Our findings demonstrate that soil animals are important as repositories of microbial biodiversity, and those at the top of the food web harbor more diverse and unique microbiomes. This hidden source of biodiversity is rarely considered in biodiversity and conservation debates and stresses the importance of preserving key soil invertebrates.

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Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

Cited by 4 publications

References 14 publications

Rampant Host Switching Shaped the Termite Gut Microbiome

Rampant Host Switching Shaped the Termite Gut Microbiome

Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment

Trophic level drives the host microbiome of soil invertebrates at a continental scale

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