Mixed transmission modes and dynamic genome evolution in an obligate animal–bacterial symbiosis

Russell, Shelbi L.; Corbett-Detig, Russell; Cavanaugh, Colleen M.

doi:10.1038/ismej.2017.10

Cited by 35 publications

(66 citation statements)

References 80 publications

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“…A comparison of the p values estimated here to other microbiome studies shows that higher p SOX have been observed in other Bathymodiolus species (mean between 2.2 x10 -3 and 3.9x10 -3 ) 25 . The average SOX and MOX nucleotide diversity estimated here is within the range of p values observed in the clam Solemya velum microbiome where the symbiont transmission mode is thought to be a mixture of vertical and horizontal transmission 40 . Furthermore, our p estimates are lower than those observed for most bacterial species in the human gut microbiome that are considered horizontally transmitted 19 .…”

Section: Sox Strains Evolve Under Purifying Selection While Mox Evolusupporting

confidence: 67%

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Picazo¹,

Ansorge

Petersen

et al. 2019

Preprint

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Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for the bacterial ecology and evolution. Vertical symbiont transmission leads to geographic isolation of the microbial population and consequently to genetic isolation of microbiotas from individual hosts. In contrast, the extent of geographic and genetic isolation of horizontally transmitted microbiota is poorly characterized.Here we show that chemosynthetic symbionts of individual Bathymodiolus brooksi mussels constitute genetically isolated populations. The reconstruction of core genome-wide strain sequences from high-resolution metagenomes revealed distinct phylogenetic clades. Nucleotide diversity and strain composition vary along the mussel lifespan and individual hosts show a high degree of genetic isolation. Our results suggest that the uptake of environmental bacteria is a restricted process in B. brooksi, where self-infection of the gill tissue results in serial founder effects during symbiont evolution. We conclude that bacterial colonization dynamics over the host life-cycle is thus an important determinant of population structure and genome evolution of horizontally transmitted symbionts.

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Section: Sox Strains Evolve Under Purifying Selection While Mox Evolusupporting

confidence: 67%

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Picazo¹,

Ansorge

Petersen

et al. 2019

Preprint

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“…Evidence of a transmission bottleneck (low Epulopiscium Hd in host Nt_050613) suggests that the detected recombination events were relatively recent in Epulopiscium evolutionary history. Even in the obligate symbiosis between the bivalve Solemya velum and its bacterial gill endosymbionts, mixed infections and recombination occurs at a high enough frequency to maintain symbiont diversity [25]. This further suggests that symbiont allele frequencies reflect a dynamic state in which populations may not reach equilibrium.…”

Section: Genetic Exchange Within the Epulopiscium Sp Type B Populationsmentioning

confidence: 99%

“…Surgeonfish most likely acquire epulos through conspecific coprophagy [23]. Unlike vertically transmitted insect endosymbionts [24], populations of horizontally transmitted obligate symbionts do not appear to be as genetically constrained by dispersal bottlenecks [25,26]. The apparent clonality of Epulopiscium sp.…”

Section: Introductionmentioning

confidence: 99%

Recombination contributes to population diversification in the polyploid intestinal symbiont Epulopiscium sp. type B

et al. 2019

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Epulopiscium sp. type B (Lachnospiraceae) is an exceptionally large, highly polyploid, intestinal symbiont of the coral reef dwelling surgeonfish Naso tonganus. These obligate anaerobes do not form mature endospores and reproduce solely through the production of multiple intracellular offspring. This likely makes them dependent on immediate transfer to a receptive host for dispersal. During reproduction, only a small proportion of Epulopiscium mother-cell DNA is inherited. To explore the impact of this unusual viviparous lifestyle on symbiont population dynamics, we investigated Epulopiscium sp. type B and their fish hosts collected over the course of two decades, at island and reef habitats near Lizard Island, Australia. Using multi-locus sequence analysis, we found that recombination plays an important role in maintaining diversity of these symbionts and yet populations exhibit linkage disequilibrium (LD). Symbiont populations showed spatial but not temporal partitioning. Surgeonfish are long-lived and capable of traveling long distances, yet the population structures of Epulopiscium suggest that adult fish tend to not roam beyond a limited locale. Codiversification analyses and traits of this partnership suggest that while symbionts are obligately dependent on their host, the host has a facultative association with Epulopiscium. We suggest that congression of unlinked markers contributes to LD estimates in this and other recombinant populations of bacteria. The findings here inform our understanding of evolutionary processes within intestinal Lachnospiraceae populations. Supplementary informationThe online version of this article (https://

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“…An intermediate mode of transmission using both vertical and horizontal transmission strategies, termed mixed-mode transmission [2,3], is reported for several associations (e.g. [9,10]) and may be the dominant context in which vertical transmission occurs in the marine environment. The vast majority of marine symbioses are horizontally transmitted [2], and the ones that undergo vertical transmission experience occasional horizontal events [11,12].…”

Section: Introductionmentioning

confidence: 99%

“…Early research concluded that symbionts are vertically transmitted based upon detection of symbiont DNA in host ovaries via PCR and bacterial cells in developing juvenile gill buds within the egg capsule [14]. Recent genomic data revealed evidence of evolutionarily frequent rates of horizontal transmission [10,15], prompting a more detailed analysis of the life history of the S. velum symbiont to compare the dynamics of these transmission modes at ecological time scales (e.g. within host tissues and environmental substrates, such as seawater and sediment).…”

Section: Introductionmentioning

confidence: 99%

Transmission strategies in a chemosynthetic symbiosis: detection and quantification of symbionts in host tissues and their environment

Russell

McCartney

2018

Proc. R. Soc. B.

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Transmission of bacteria vertically through host tissues ensures offspring acquire symbionts; however, horizontal transmission is an effective strategy for many associations and plays a role in some vertically transmitted symbioses. The bivalve Solemya velum and its gammaproteobacterial chemosynthetic symbionts exhibit evolutionary evidence of both transmission modes, but the dominant strategy on an ecological time scale is unknown. To address this, a specific primer set was developed and validated for the S. velum symbiont using a novel workflow called specific marker design (SMD). Symbionts were quantified in spawned eggs and sediment and seawater samples from S. velum habitats with qPCR. Each egg was estimated to contain 50-100 symbiont genomes. By contrast, symbiont DNA was found at low abundance/occurrence in sediment and seawater, often co-occurring with host mitochondrial DNA, obscuring its origin. To ascertain when eggs become infected, histological sections of S. velum tissues were labelled for symbiont 16S rRNA via in situ hybridization. This revealed symbionts in the ovary walls and mature oocytes, suggesting association in late oogenesis. These data support the hypothesis that S. velum symbionts are vertically transmitted every host generation, thus genetic signatures of horizontal transmission are driven by ecologically infrequent events. This knowledge furthers our understanding of vertical and horizontal mode integration and provides insights across animal-bacterial chemosynthetic symbioses.rspb.royalsocietypublishing.org Proc. R. Soc. B 285: 20182157

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Mixed transmission modes and dynamic genome evolution in an obligate animal–bacterial symbiosis

Cited by 35 publications

References 80 publications

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Recombination contributes to population diversification in the polyploid intestinal symbiont Epulopiscium sp. type B

Transmission strategies in a chemosynthetic symbiosis: detection and quantification of symbionts in host tissues and their environment

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