The winnowing: establishing the squid–vibrio symbiosis

Nyholm, Spencer V.; McFall‐Ngai, Margaret J.

doi:10.1038/nrmicro957

Cited by 698 publications

(704 citation statements)

References 73 publications

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“…Colonization from the surrounding environment is thought to be one of the primary mechanisms of microbiota acquisition for fish (Nayak, 2010), and is found in many other animal-microbe symbioses, including the Hawaiian bobtail squid and their luminescent Vibrio fischeri symbionts. In that system, V. fischeri are found at very low abundances in the surrounding aquatic habitat (o0.1% of bacterioplankton), yet exclusive colonization of squid light organs is achieved through specific mechanisms employed by both symbionts and hosts (Nyholm and McFall-Ngai, 2004). Although Trinidadian guppies likely acquire their symbionts from their environment, we found no correlations between gut and environmental bacterial OTU abundance from the same location when examined across Guanapo stream sites.…”

Section: Drivers Of Natural Microbiome Compositioncontrasting

confidence: 43%

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

et al. 2015

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Diverse microbial consortia profoundly influence animal biology, necessitating an understanding of microbiome variation in studies of animal adaptation. Yet, little is known about such variability among fish, in spite of their importance in aquatic ecosystems. The Trinidadian guppy, Poecilia reticulata, is an intriguing candidate to test microbiome-related hypotheses on the drivers and consequences of animal adaptation, given the recent parallel origins of a similar ecotype across streams. To assess the relationships between the microbiome and host adaptation, we used 16S rRNA amplicon sequencing to characterize gut bacteria of two guppy ecotypes with known divergence in diet, life history, physiology and morphology collected from low-predation (LP) and high-predation (HP) habitats in four Trinidadian streams. Guts were populated by several recurring, core bacteria that are related to other fish associates and rarely detected in the environment. Although gut communities of lab-reared guppies differed from those in the wild, microbiome divergence between ecotypes from the same stream was evident under identical rearing conditions, suggesting host genetic divergence can affect associations with gut bacteria. In the field, gut communities varied over time, across streams and between ecotypes in a stream-specific manner. This latter finding, along with PICRUSt predictions of metagenome function, argues against strong parallelism of the gut microbiome in association with LP ecotype evolution. Thus, bacteria cannot be invoked in facilitating the heightened reliance of LP guppies on lower-quality diets. We argue that the macroevolutionary microbiome convergence seen across animals with similar diets may be a signature of secondary microbial shifts arising some time after host-driven adaptation.

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Section: Drivers Of Natural Microbiome Compositioncontrasting

confidence: 43%

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

et al. 2015

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“…Only members of the species V. fischeri are allowed to adhere to the underside of the squid and to induce apoptosis in the tissue that will become the light organ. And only when they have reached a certain density do they begin to emit light (Nyholm & McFall-Ngai 2004;Visick & Ruby 2006).…”

Section: Developmental Symbiosismentioning

confidence: 99%

Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy

Gilbert

McDonald

Boyle

et al. 2010

Phil. Trans. R. Soc. B

129

110

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Evolutionary developmental biology is based on the principle that evolution arises from hereditable changes in development. Most of this new work has centred on changes in the regulatory components of the genome. However, recent studies (many of them documented in this volume) have shown that development also includes interactions between the organism and its environment. One area of interest concerns the importance of symbionts for the production of the normal range of phenotypes. Many, if not most, organisms have 'outsourced' some of their developmental signals to a set of symbionts that are expected to be acquired during development. Such intimate interactions between species are referred to as codevelopment, the production of a new individual through the coordinated interactions of several genotypically different species. Within the past 2 years, several research programmes have demonstrated that such codevelopmental schemes can be selected. We will focus on symbioses in coral reef cnidarians symbiosis, pea aphids and cactuses, wherein the symbiotic system provides thermotolerance for the composite organism.

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“…In leguminous plants, infection with symbiotic Rhizobium induces nodule formation in the root (Perret et al, 2000;Oldroyd and Downie, 2008). In Euprymna squids, infection with luminescent Vibrio fischeri is required for normal morphogenesis of the symbiotic light organ (McFall-Ngai and Ruby, 1991;Nyholm and McFall-Ngai, 2004). Whether or not the Burkholderia symbiont is involved in the formation of the host symbiotic organ is of interest, deserving future experimental and developmental studies on symbiotic and aposymbiotic insects.…”

Section: Lch90 From Leptocorisa Chinensismentioning

confidence: 99%

“…On the other hand, environmental symbiont transmission, wherein newborn host organisms acquire their mutualistic partners from environmental microbial pool every generation, has been known from diverse marine invertebrates including luminescent squids (Nyholm and McFall-Ngai, 2004), photosynthetic corals (Baker, 2003), chemoautotrophic tubeworms (Dubilier et al, 2008) and many others. In the aquatic ecosystem, free-living symbionts are protected from environmental stresses such as UV irradiation and desiccation that must be detrimental to free-living symbionts in the terrestrial ecosystem, to which the paucity of environmental symbiont transmission among insects may be relevant.…”

Section: Introductionmentioning

confidence: 99%

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

2010

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Here, we investigated 124 stinkbug species representing 20 families and 5 superfamilies for their Burkholderia gut symbionts, of which 39 species representing 6 families of the superfamilies Lygaeoidea and Coreoidea were Burkholderia-positive. Diagnostic PCR surveys revealed high frequencies of Burkholderia infection in natural populations of the stinkbugs, and substantial absence of vertical transmission of Burkholderia infection to their eggs. In situ hybridization confirmed localization of the Burkholderia in their midgut crypts. In the lygaeoid and coreoid stinkbugs, development of midgut crypts in their alimentary tract was coincident with the Burkholderia infection, suggesting that the specialized morphological configuration is pivotal for establishment and maintenance of the symbiotic association. The Burkholderia symbionts were easily isolated as pure culture on standard microbiological media, indicating the ability of the gut symbionts to survive outside the host insects. Molecular phylogenetic analysis showed that the gut symbionts of the lygaeoid and coreoid stinkbugs belong to a b-proteobacterial clade together with Burkholderia isolates from soil environments and Burkholderia species that induce plant galls. On the phylogeny, the stinkbug-associated, environmental and gall-forming Burkholderia strains did not form coherent groups, indicating host-symbiont promiscuity among these stinkbugs. Symbiont culturing revealed that slightly different Burkholderia genotypes often coexist in the same insects, which is also suggestive of host-symbiont promiscuity. All these results strongly suggest an ancient but promiscuous host-symbiont relationship between the lygaeoid/coreoid stinkbugs and the Burkholderia gut symbionts. Possible mechanisms as to how the environmentally transmitted promiscuous symbiotic association has been stably maintained in the evolutionary course are discussed.

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The winnowing: establishing the squid–vibrio symbiosis

Cited by 698 publications

References 73 publications

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

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