Methanogenic symbionts of anaerobic ciliates are host and habitat specific.

The association between anaerobic ciliates and methanogenic archaea has been recognized for over a century. Nevertheless, knowledge of these associations is limited to a few ciliate species, and so the identification of patterns of host-symbiont specificity has been largely speculative. In this study, we integrated microscopy and genetic identification to survey the methanogenic symbionts of 32 free-living anaerobic ciliate species, mainly from the order Metopida.

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.

Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation.

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 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 , which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses.

Geography, not lifestyle, explains the population structure of free-living and host-associated deep-sea hydrothermal vent snail symbionts.

Background: Marine symbioses are predominantly established through horizontal acquisition of microbial symbionts from the environment. However, genetic and functional comparisons of free-living populations of symbionts to their host-associated counterparts are sparse. Here, we assembled the first genomes of the chemoautotrophic gammaproteobacterial symbionts affiliated with the deep-sea snail Alviniconcha hessleri from two separate hydrothermal vent fields of the Mariana Back-Arc Basin.

Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snail Alviniconcha adamantis from the Mariana Arc.

Chemosynthetic animal-microbe symbioses sustain hydrothermal vent communities in the global deep sea. In the Indo-Pacific Ocean, hydrothermal ecosystems are often dominated by gastropod species of the genus Alviniconcha, which live in association with chemosynthetic Gammaproteobacteria or Campylobacteria. While the symbiont genomes of most extant Alviniconcha species have been sequenced, no genome information is currently available for the gammaproteobacterial endosymbiont of Alviniconcha adamantis-a comparatively shallow living species that is thought to be the ancestor to all other present Alviniconcha lineages.

Horizontal transmission enables flexible associations with locally adapted symbiont strains in deep-sea hydrothermal vent symbioses.

SignificanceIn marine ecosystems, transmission of microbial symbionts between host generations occurs predominantly through the environment. Yet, it remains largely unknown how host genetics, symbiont competition, environmental conditions, and geography shape the composition of symbionts acquired by individual hosts. To address this question, we applied population genomic approaches to four species of deep-sea hydrothermal vent snails that live in association with chemosynthetic bacteria.

Anaerobic ciliates as a model group for studying symbioses in oxygen-depleted environments.

Anaerobiosis has independently evolved in multiple lineages of ciliates, allowing them to colonize a variety of anoxic and oxygen-depleted habitats. Anaerobic ciliates commonly form symbiotic relationships with various prokaryotes, including methanogenic archaea and members of several bacterial groups. The hypothesized functions of these ecto- and endosymbionts include the symbiont utilizing the ciliate's fermentative end products to increase the host's anaerobic metabolic efficiency, or the symbiont directly providing the host with energy by denitrification or photosynthesis.

Divergent paths in the evolutionary history of maternally transmitted clam symbionts.

Vertical transmission of bacterial endosymbionts is accompanied by virtually irreversible gene loss that results in a progressive reduction in genome size. While the evolutionary processes of genome reduction have been well described in some terrestrial symbioses, they are less understood in marine systems where vertical transmission is rarely observed. The association between deep-sea vesicomyid clams and chemosynthetic Gammaproteobacteria is one example of maternally inherited symbioses in the ocean.

Global 16S rRNA diversity of provannid snail endosymbionts from Indo-Pacific deep-sea hydrothermal vents.

Symbioses between invertebrate animals and chemosynthetic bacteria build the foundation of deep-sea hydrothermal ecosystems worldwide. Despite the importance of these symbioses for ecosystem functioning, the diversity of symbionts within and between host organisms and geographic regions is still poorly understood. In this study we used 16S rRNA amplicon sequencing to determine the diversity of gill endosymbionts in provannid snails of the genera Alviniconcha and Ifremeria, which are key species at deep-sea hydrothermal vents in the Indo-Pacific Ocean.

Differential patterns of connectivity in Western Pacific hydrothermal vent metapopulations: A comparison of biophysical and genetic models.

Hydrothermal ecosystems face threats from planned deep-seabed mining activities, despite the fact that patterns of realized connectivity among vent-associated populations and communities are still poorly understood. Since populations of vent endemic species depend on larval dispersal to maintain connectivity and resilience to habitat changes, effective conservation strategies for hydrothermal ecosystems should include assessments of metapopulation dynamics. In this study, we combined population genetic methods with biophysical models to assess strength and direction of gene flow within four species of the genus (.

Cooccurring Activities of Two Autotrophic Pathways in Symbionts of the Hydrothermal Vent Tubeworm .

Genome and proteome data predict the presence of both the reductive citric acid cycle (rCAC; also called the reductive tricarboxylic acid cycle) and the Calvin-Benson-Bassham cycle (CBB) in " Endoriftia persephonae," the autotrophic sulfur-oxidizing bacterial endosymbiont from the giant hydrothermal vent tubeworm Riftia pachyptila. We tested whether these cycles were differentially induced by sulfide supply, since the synthesis of biosynthetic intermediates by the rCAC is less energetically expensive than that by the CBB. R.

Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails.

Despite significant advances in our understanding of speciation in the marine environment, the mechanisms underlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus.

Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails.

Symbioses between invertebrate animals and chemosynthetic bacteria form the basis of hydrothermal vent ecosystems worldwide. In the Lau Basin, deep-sea vent snails of the genus Alviniconcha associate with either Gammaproteobacteria (A. kojimai, A.

Genomics of New Ciliate Lineages Provides Insight into the Evolution of Obligate Anaerobiosis.

Oxygen plays a crucial role in energetic metabolism of most eukaryotes. Yet adaptations to low-oxygen concentrations leading to anaerobiosis have independently arisen in many eukaryotic lineages, resulting in a broad spectrum of reduced and modified mitochondrion-related organelles (MROs). In this study, we present the discovery of two new class-level lineages of free-living marine anaerobic ciliates, Muranotrichea, cl.

The Bacterial Symbionts of Closely Related Hydrothermal Vent Snails With Distinct Geochemical Habitats Show Broad Similarity in Chemoautotrophic Gene Content.

Symbiosis has evolved between a diversity of invertebrate taxa and chemosynthetic bacterial lineages. At the broadest level, these symbioses share primary function: the bacterial symbionts use the energy harnessed from the oxidation of reduced chemicals to power the fixation of inorganic carbon and/or other nutrients, providing the bulk of host nutrition. However, it is unclear to what extent the ecological niche of the host species is influenced by differences in symbiont traits, particularly those involved in chemoautotrophic function and interaction with the geochemical environment.

The Significance of Microbial Symbionts in Ecosystem Processes.

It is increasingly accepted that the microbial symbionts of eukaryotes can have profound effects on host ecology and evolution. However, the relative contribution that they make directly to ecosystem processes, like energy and nutrient flows, is less explicitly acknowledged and, in many cases, only poorly constrained. Here, I explore the idea that, in some habitats, host-associated microbes may have an outsized role in ecosystem processes relative to functionally equivalent free-living microbes due to key aspects of the physiology, ecology, and evolution of symbiotic interactions.

Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes.

Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry.

Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean.

In addition to the cyanobacterial N2-fixers (diazotrophs), there is a high nifH gene diversity of non-cyanobacterial groups present in marine environments, yet quantitative information about these groups is scarce. N2 fixation potential (nifH gene expression), diversity and distributions of the uncultivated diazotroph phylotype γ-24774A11, a putative gammaproteobacterium, were investigated in the western South Pacific Ocean. γ-24774A11 gene copies correlated positively with diazotrophic cyanobacteria, temperature, dissolved organic carbon and ambient O2 saturation, and negatively with depth, chlorophyll a and nutrients, suggesting that carbon supply, access to light or inhibitory effects of DIN may control γ-24774A11 abundances.

Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses.

Deep-sea hydrothermal vents are populated by dense communities of animals that form symbiotic associations with chemolithoautotrophic bacteria. To date, our understanding of which factors govern the distribution of host/symbiont associations (or holobionts) in nature is limited, although host physiology often is invoked. In general, the role that symbionts play in habitat utilization by vent holobionts has not been thoroughly addressed.

Seasonal change in the abundance of Synechococcus and multiple distinct phylotypes in Monterey Bay determined by rbcL and narB quantitative PCR.

Synechococcus is a cosmopolitan marine cyanobacterial genus, and is often the most abundant picocyanobacterial genus in coastal waters. Little is known about Synechococcus seasonal dynamics in coastal zones highly impacted by upwelling. This was investigated by collecting seasonal samples from an upwelling-impacted Monterey Bay (MB) monitoring station M0, in parallel with measurements of oceanographic conditions during 2006-2008.

Thermodynamics and kinetics of sulfide oxidation by oxygen: a look at inorganically controlled reactions and biologically mediated processes in the environment.

The thermodynamics for the first electron transfer step for sulfide and oxygen indicates that the reaction is unfavorable as unstable superoxide and bisulfide radical ions would need to be produced. However, a two-electron transfer is favorable as stable S(0) and peroxide would be formed, but the partially filled orbitals in oxygen that accept electrons prevent rapid kinetics. Abiotic sulfide oxidation kinetics improve when reduced iron and/or manganese are oxidized by oxygen to form oxidized metals which in turn oxidize sulfide.

Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain.

Nitrogen (N2)-fixing microorganisms (diazotrophs) are an important source of biologically available fixed N in terrestrial and aquatic ecosystems and control the productivity of oligotrophic ocean ecosystems. We found that two major groups of unicellular N2-fixing cyanobacteria (UCYN) have distinct spatial distributions that differ from those of Trichodesmium, the N2-fixing cyanobacterium previously considered to be the most important contributor to open-ocean N2 fixation. The distributions and activity of the two UCYN groups were separated as a function of depth, temperature, and water column density structure along an 8000-kilometer transect in the South Pacific Ocean.

In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii.

The diazotrophic cyanobacterium Crocosphaera watsonii supplies fixed nitrogen (N) to N-depleted surface waters of the tropical oceans, but the factors that determine its distribution and contribution to global N(2) fixation are not well constrained for natural populations. Despite the heterogeneity of the marine environment, the genome of C. watsonii is highly conserved in nucleotide sequence in contrast to sympatric planktonic cyanobacteria.

Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon.

The spatial heterogeneity of diversity and abundance of diazotrophs were investigated off the Vietnamese coast in the South China Sea (SCS). The study area extended from the Mekong River plume to the shelf region and beyond to stations extending to 1700 m depth. The SCS diazotroph community, based on nifH gene diversity, had components closely related to sequences from open ocean, estuarine, saltmarsh and microbial mat communities.