Biology subjects

Beinart, R.

Publications and source records attributed to Beinart, R..

3 recordsLinked to original sources

bioRxiv2021

Host-symbiont population genomics provide insights into partner fidelity, transmission mode and habitat adaptation in deep-sea hydrothermal vent snails

Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species level associations that might influence genetic structuring, connectivity and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across a ~800 km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor wide-spread genetic connectivity and ecological resilience unless physical dispersal barriers are present. Significance StatementSymbiont composition in horizontally transmitted symbioses is influenced by a combination of host genetics, environmental conditions and geographic barriers. Yet the relative importance of these factors and the effects of adaptive versus neutral evolutionary forces on symbiont population structure remain unknown in the majority of marine symbioses. To address these questions, we applied population genomic approaches in four species of deep-sea hydrothermal vent snails that live in obligate association with chemosynthetic bacteria. Our analyses show that host genetics plays a minor role compared to environment for symbiont strain composition despite specificity to symbiont species and corroborate a long-standing hypothesis that vent invertebrates affiliate with locally adapted symbiont strains to cope with the variable habitat conditions characterizing hydrothermal vents.

molecular biology↗

bioRxiv2020

Differences in cofactor, oxygen and sulfur requirements influence niche adaptation in deep-sea vesicomyid clam symbioses

Vertical transmission of bacterial endosymbionts is accompanied by virtually irreversible gene loss that can provide insights into adaptation to divergent ecological niches. While patterns of genome reduction have been well described in some terrestrial symbioses, they are less understood in marine systems where vertical transmission is relatively rare. The association between deep-sea vesicomyid clams and chemosynthetic Gammaproteobacteria is one example of maternally inherited symbioses in the ocean. Differences in nitrogen and sulfur physiology between the two dominant symbiont groups, Ca. Ruthia and Ca. Vesicomyosocius, have been hypothesized to influence niche exploitation, which likely affects gene content evolution in these symbionts. However, genomic data are currently limited to confirm this assumption. In the present study we sequenced and compared 11 vesicomyid symbiont genomes with existing assemblies for Ca. Vesicomyosocius okutanii and Ca. Ruthia magnifica. Our analyses indicate that the two vesicomyid symbiont groups have a common core genome related to chemosynthetic metabolism, but differ in their potential for nitrate respiration and flexibility to environmental sulfide concentrations. Moreover, Ca. Vesicomyosocius and Ca. Ruthia have different enzymatic requirements for cobalamin and nickel and show contrasting capacities to acquire foreign genetic material. Tests for site-specific positive selection in metabolic candidate genes imply that the observed physiological differences are adaptive and thus likely correspond to ecological niches available to each symbiont group. These findings highlight the role of niche differentiation in creating divergent paths of reductive genome evolution in vertically transmitted symbionts.

genomics↗

bioRxiv2019

Horizontal transmission and recombination maintain forever young bacterial symbiont genomes

Bacterial symbionts bring a wealth of functions to the associations they participate in, but by doing so, they endanger the genes and genomes underlying these abilities. When bacterial symbionts become obligately associated with their hosts, their genomes are thought to decay towards an organelle-like fate due to decreased homologous recombination and inefficient selection. However, numerous associations exist that counter these expectations, especially in marine environments, possibly due to ongoing horizontal gene flow. Despite extensive theoretical treatment, no empirical study thus far has connected these underlying population genetic processes with long-term evolutionary outcomes. By sampling marine chemosynthetic bacterial-bivalve endosymbioses that range from primarily vertical to strictly horizontal transmission, we tested this canonical theory. We found that transmission mode strongly predicts homologous recombination rates, and that exceedingly low recombination rates are associated with moderate genome degradation in the marine symbionts with nearly strict vertical transmission. Nonetheless, even the most degraded marine endosymbiont genomes are occasionally horizontally transmitted and are much larger than their terrestrial insect symbiont counterparts. Therefore, horizontal transmission and recombination enable efficient natural selection to maintain intermediate symbiont genome sizes and substantial functional genetic variation. Author summarySymbiotic associations between bacteria and eukaryotes are ubiquitous in nature and have contributed to the evolution of radically novel phenotypes and niches for the involved partners. New metabolic or physiological capacities that arise in these associations are typically encoded by the bacterial symbiont genomes. However, the association itself endangers the retention of bacterial genomic coding capacity. Endosymbiont genome evolution theory predicts that when bacterial symbionts become restricted to host tissues, their populations cannot remove deleterious mutations efficiently. This ultimately results in their genomes degrading to small, function-poor states, reminiscent of organellar genomes. However, many ancient marine endosymbionts do not fit this prediction, but instead retain relatively large, gene-rich genomes, indicating that the evolutionary dynamics of this process need more thorough characterization. Here we show that on-going symbiont gene flow via horizontal transmission between bivalve hosts and recombination among divergent gammaproteobacterial symbiont lineages are sufficient to maintain large and dynamic bacterial symbiont genomes. These findings indicate that many obligately associated symbiont genomes may not be as isolated from one another as previously assumed and are not on a one way path to degradation.

evolutionary biology↗