Biology subjects

Beinart, R. A.

Publications and source records attributed to Beinart, R. A..

8 recordsLinked to original sources

bioRxiv2026

Distinct genomic adaptations of the methanogenic archaeal genus Methanocorpusculum to symbiosis with animals and protists

Most of our understanding of endosymbiosis originates from the bacterial endosymbionts of multicellular, terrestrial hosts, which represent habitats with dramatically different selective pressures than inside a protist cell. Methanogenic archaea from the genus Methanocorpusculum are among the few known intracellular archaea and form unique symbioses with both animal and protist hosts, providing a unique opportunity to contrast symbiont evolution and function in very distinct host types. Here, we conducted phylo- and pangenomic analyses on 106 Methanocorpusculum strains originating from animal and ciliate hosts as well as environmental habitats. We recovered two divergent clades corresponding to animal gut-associated and intracellular ciliate-associated/environmental lineages and found that ciliate-associated and environmental Methanocorpusculum are virtually indistinguishable functionally and phylogenetically. Ciliate-associated symbionts retained broad biosynthetic capacity and encoded functions related to osmotic stress tolerance and adhesion within the host cell, while animal gut-associated symbionts exhibited patterns of genome streamlining and nutrient scavenging consistent with host supply and immune adaptation. Our findings illuminate how the contrasting selective pressures of protists and animal hosts have driven divergent evolutionary and functional strategies in congeneric archaeal symbionts.

microbiology↗

bioRxiv2025

A meta-analysis of environmental sequencing data reveals the global distribution and hidden diversity of marine anaerobic ciliates

Anaerobic protists are diverse, ecologically important members of anoxic microbial communities, acting as grazers, nutrient cyclers, and partners in multi-domain associations, yet remain understudied relative to anaerobic prokaryotes. Ciliates are particularly abundant and diverse in anoxia, but their global diversity and distribution are largely unknown. Here, we conducted a meta-analysis of public 18S rDNA datasets, along with one dataset generated here, to assess the global diversity and ecology of marine anaerobic ciliates. Using a novel pipeline, we processed 2854 samples from 42 studies spanning 19 habitat types. We recovered 3196 anaerobic ciliate amplicon sequence variants (ASVs) across all described lineages. Based on clade-specific divergence thresholds derived from phylogenetic distances, 28.4-46.3% of ASVs qualified as novel. Most sequences belonged to the poorly described plagiopylean family Epalxellidae, suggesting a large reservoir of undescribed diversity in this clade. Community comparisons revealed close phylogenetic similarities between some shallow-water and deep-sea assemblages, suggesting that shared redox conditions may shape communities more than water depth. Our results demonstrate that marine anaerobic ciliates are globally distributed, taxonomically diverse, and rich in novel lineages. This study provides a framework for leveraging environmental sequencing data to better understand the diversity and ecology of neglected protist lineages and under-sampled habitats.

microbiology↗

bioRxiv2025

Evolutionary convergence and trophic diversity in hot vent and cold seep shrimps showcase a continuum of symbiosis

Convergent evolution offers a powerful lens through which to examine the selective forces shaping life in extreme environments. In deep-sea hot vents and cold seeps, invertebrates have independently evolved symbioses with chemosynthetic bacteria, but repeated origins of such associations within a family remain rare. Here, we investigate the evolutionary emergence of chemosymbiosis in the shrimp family Alvinocarididae across 22 species collected globally. Electron microscopy identified a gradient of epibiotic bacterial colonization within the cephalothoracic cavity, ranging from absent to dense filamentous mats, suggesting distinct trophic strategies. Isotope and lipid trophic markers confirmed difference in reliance on chemosynthetic production among sympatric species with different bacterial colonization from a single vent. Phylogenetic analysis reveals at least two independent origins of chemosymbiosis, suggesting evolutionary convergence. Microhabitat association data further show that symbiotic phenotypes are most common in shrimps occupying the hottest, most geofluid-enriched microhabitats, though exceptions suggest contributions from additional ecological or physiological constraints. Our findings reveal many alvinocaridids as gradually evolving towards symbiosis, highlighting the importance of intermediate cases to understand the pathways to chemosymbiosis. This study contributes to a broader understanding of the predictability of evolutionary outcomes in distinct habitats such as vents, with broader implications for resilience of deep-sea ecosystems.

evolutionary biology↗

bioRxiv2025

Population genomic insights into syntrophic symbioses between marine anaerobic ciliates and intracellular methanogens

Symbiotic interactions are an ecologically and evolutionary significant phenomenon pertaining to virtually every organism on Earth. For eukaryotes inhabiting extreme environments, syntrophic symbioses with microbes may be key to successfully colonizing new niches, such as globally expanding oxygen-depleted habitats. Multi-domain symbioses between microbial eukaryotes and intracellular methanogenic archaea are crucial to understanding the origins and mechanisms of eukaryotic anaerobiosis. Nearly all anaerobic ciliates, ecologically important protists found in diverse oxygen-depleted environments, host methanogenic endosymbionts, sometimes alongside bacterial partners, that facilitate their anaerobic metabolism. Although vertical symbiont transmission necessarily occurs during ciliate cell division, symbionts might occasionally be acquired horizontally. However, patterns of host-symbiont specificity and intraspecific variability remain poorly understood. Here, we present the first intra-specific genomic analysis of both host and symbionts in such partnerships, providing key insights into the fidelity of eukaryotic-prokaryotic liaisons in anoxia. We assessed the symbiont-host co-diversification and genetic variation across eleven populations of a single undescribed Metopus species hosting Methanocorpusculum cultured from intertidal sediment locations separated by meters to 1000s of kilometers. Our results show incongruency in host mitochondrial and symbiont phylogenies, indicating a mixed transmission mode. On a genomic level, both host and symbiont populations formed distinct location-specific clusters exhibiting no signs of isolation-by-distance. Instead, ecological factors appear to have driven population genomic divergence at least partly and likely led to differences in metabolic traits. Symbiont comparative and population genomics enable us to further comprehend the complex nature of these multi-partner syntrophic symbioses, crucial to interpreting cell-cell interactions across the domains of life.

microbiology↗

bioRxiv2025

Contrasting genomic responses of hydrothermal vent animals and their symbionts to population decline after the Hunga volcanic eruption

Genetic bottlenecks are evolutionary events that reduce the effective size and diversity of natural populations, often limiting a populations ability to adapt to environmental change. Given the accelerating human impact on ecosystems worldwide, understanding how populations evolve after a genetic bottleneck is becoming increasingly important for species conservation. Ash deposits from the 2022 Hunga volcanic eruption in the Southwest Pacific led to a drastic decline of animal symbioses associated with hydrothermal vents in this region, allowing insights into the effects of population bottlenecks in the deep sea. Here, we applied metagenomic sequencing to pre- and post-eruption samples of mollusk-microbial symbioses from the Lau Basin to investigate patterns of genetic variation and effective population size. Our data indicate that animal host populations currently show only small changes in genome-wide diversity but in most cases experienced a long-term decline in effective size that was likely intensified by the volcanic impact. By contrast, symbiont populations exhibited a notable decrease in genomic variation, including loss of certain habitat-specific strains. However, detection of environmental symbiont sequences suggests that lost strain diversity might be recovered from the free-living symbiont pool. The differences between host and symbiont populations might be related to their contrasting genetic structures and levels of gene flow, although the full extent of population bottlenecks in the host animals might only be recognizable after a few generations. These results add to our understanding of the evolutionary dynamics of animal-microbe populations following a natural disturbance and help assess their resilience to potential future anthropogenic impacts.

evolutionary biology↗

bioRxiv2025

Phage interactions may contribute to the population structure and dynamics of hydrothermal vent microbial symbionts

Deep-sea hydrothermal vent ecosystems are sustained by chemoautotrophic bacteria that symbiotically provide organic matter to their animal hosts through the oxidation of chemical reductants in vent fluids. Hydrothermal vents also support unique viral communities that often exhibit high host-specificity and frequently integrate into host genomes as prophages; however, little is known about the role of viruses in influencing the chemosynthetic symbionts of vent foundation fauna. Here, we present a comprehensive examination of contemporary lysogenic and lytic bacteriophage infections, auxiliary metabolic genes, and CRISPR spacers associated with the intracellular bacterial endosymbionts of snails and mussels at hydrothermal vents in the Lau Basin (Tonga). Our investigation of contemporary phage infection among bacterial symbiont species and across distant vent locations indicated that each symbiont species interacts with different phage species across a large geographic range. However, our analysis of historical phage interactions via assessment of CRISPR spacer content suggested that phages may contribute to strain-level variation within a symbiont species. Surprisingly, prophages were absent from almost all symbiont genomes, suggesting that phage interactions with intracellular symbionts may differ from free-living microbes at vents. Altogether, these findings suggest that species-specific phages play a key role in regulating chemosynthetic symbionts via lytic infections, potentially shaping strain-level diversity and altering the composition and dynamics of symbiont populations.

microbiology↗

bioRxiv2024

Divergent marine anaerobic ciliates harbor closely related Methanocorpusculum endosymbionts

Ciliates are a diverse group of protists known for their ability to establish various partnerships and thrive in a wide variety of oxygen-depleted environments. Most anaerobic ciliates harbor methanogens, one of the few known archaea living intracellularly. These methanogens increase the metabolic efficiency of host fermentation via syntrophic use of host end-product in methanogenesis. Despite the ubiquity of these symbioses in anoxic habitats, patterns of symbiont specificity and fidelity are not well known. We surveyed two unrelated, commonly found groups of anaerobic ciliates, the Plagiopylea and Metopida, isolated from anoxic marine sediments. We sequenced host 18S rRNA and symbiont 16S rRNA marker genes as well as the symbiont ITS region from our cultured ciliates to identify hosts and their associated methanogenic symbionts. We found that marine ciliates from both of these co-occurring, divergent groups harbor closely related yet distinct intracellular archaea within the Methanocorpusculum genus. The symbionts appear to be stable at the host species level, but at higher taxonomic levels, there is evidence that symbiont replacements have occurred. Gaining insight into this unique association will deepen our understanding of the complex transmission modes of marine microbial symbionts, and the mutualistic microbial interactions occurring across domains of life.

microbiology↗

bioRxiv2022

Host mixotrophy, habitat stability and recombination may all decrease geographic differentiation between symbiont populations in Western Pacific deep-sea mussels

The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains, it is unknown whether these patterns are universal and how differences in ecological characteristics among host-symbiont associations influence the genomic structure of symbiont populations. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses. Bathymodiolus septemdierum lives in close symbiotic relationship with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with less exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum show structuring by geographic location, but that the dominant symbiont strain is uncorrelated with vent site. These patterns are in contrast to co-occurring Alviniconcha and Ifremeria symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. Our results suggest that relative habitat homogeneity combined with sufficient symbiont dispersal and genomic mixing might promote persistence of similar symbiont strains across geographic locations, while mixotrophy might decrease selective pressures on the host to affiliate with locally adapted symbiont strains. Overall, these data contribute to our understanding of the potential mechanisms influencing symbiont population structure across a spectrum of marine microbial symbioses that vary in ecological niche and relative host dependency.

evolutionary biology↗