Colonial Tube-Dwelling Ciliates Influence Methane Cycling and Microbial Diversity within Methane Seep Ecosystems

Abstract

In a variety of marine ecosystems, microbial eukaryotes play important ecological roles; however, our knowledge of their importance in deep-sea methane seep ecosystems is limited. Microbial eukaryotes have the potential to influence microbial community composition and diversity by creating habitat heterogeneity, and may contribute to carbon cycling through grazing or symbiotic associations with microorganisms. In this study, we characterized the distribution, substrate variability and ecology of a particular group of microbial eukaryotes, known as folliculinid ciliates, at methane seeps along the eastern Pacific margin. Folliculinid ciliates were recently recognized as an abundant and ecologically important component of hydrothermal vent ecosystems, but their ecology in methane seeps has not been examined. Folliculinid ciliates inhabited methane seeps from Costa Rica to Oregon, suggesting a broad distribution in the eastern Pacific. Using phylogenetic analyses of the 18S rRNA gene, two different species of folliculinid were identified and are formally described here. Folliculinids occupied a range of physical substrates, including authigenic carbonate rocks, shells of dead vesicomyid clams, polychaete tubes and gastropod shells. Molecular analysis of the folliculinid-associated microorganisms (16S rRNA and particular methane monoxygenase) revealed that these ciliates not only influence overall microbial diversity, but also have a specific relationship with bacteria in the "Deep sea-2" methanotroph clade. Natural 13 δ C isotope signatures of the folliculinids (−35 ) and their 13 C-enrichment patterns in shipboard 13 CH 4 stable isotope-probing experiments indicated these ciliates and their associated microbes are involved in cycling methane-derived carbon. Folliculinids were significantly enriched in 13 C after the addition of 13 CH 4 over short-term (3-8 day) incubations. Together, these results suggest that folliculinid ciliates represent a previously overlooked contributor to the ecology and biogeochemical cycling at deep-sea methane seep ecosystems.

Genetic Diversity, Community Assembly, and Shaping Factors of Benthic Microbial Eukaryotes in Dongshan Bay, Southeast China

“…It has been previously shown that the benthic prokaryotic community was driven partially by the grain size composition of the sediment ( Dang et al, 2010 ). Benthic microbial eukaryotes are composed of heterotrophic groups, including ciliates and heterotrophic nanoflagellates, that prey on prokaryotes ( Fenchel, 1978 ; Pasulka et al, 2017 ). Thus, the changes of prokaryotic communities due to grain size composition might further influence the grazers.…”

“…For example, in tidal flats, diatoms form a major component of microphytobenthos on sediments and are major players in nutrient cycling and provide a food resource to larger grazers ( Lohrer et al, 2004 ; Evrard et al, 2012 ). Generally, the abundances of sediment bacteria are several orders of magnitude higher than those in the pelagic environments ( Rublee, 1982 ), so do the bacterial productions ( Starink et al, 1996 ), and grazing of heterotrophic microbial eukaryotes (e.g., heterotrophic nanoflagellates and ciliates) on bacteria was proposed to be the primary cause of bacterial mortality ( Fenchel, 1978 ; Pasulka et al, 2017 ). In addition, the abundances of some groups of microbial eukaryotes, e.g., nanoflagellates and ciliates, may even exceed those of the overlaying sea water ( Wickham et al, 2000 ; Meng et al, 2011 ).…”

Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts

“…Interestingly, MMG2 bacteria have been reported from other marine hosts based on 16S rRNA and pmoA gene sequencing, although their abundances appear to generally be considerably lower than in the Campeche sponges (Supplementary Figures S3 and S4). MMG2-related sequences were described from ciliates collected at methane seeps along the eastern Pacific coast (1.7–9.7% of the ciliate bacterial community based on 16S rRNA tag sequencing) [63], and the squat lobster Shinkaia crosnieri from hydrothermal vents off Japan (1.7–12.0% of 16S rRNA clones), [64]. MMG2 sequences were also found in two sponge species: (i) an unidentified poecilosclerid sponge from seeps in the Gulf of Mexico that is morphologically distinct from our samples [28], and (ii) Cladorhiza methanophila from mud volcanoes off Barbados (16–25% based on 16S rRNA tag sequencing [25]).…”

Lava Flows Erupted in 1996 on North Gorda Ridge Segment and the Geology of the Nearby Sea Cliff Hydrothermal Vent Field From 1-M Resolution AUV Mapping

“…The extent of the tube worm clumps is ∼140 m by ∼90 m, elongate parallel to the axis. The nearest vent fauna to the active chimneys are mats ( Figure 9F) of blue ciliate Eufolliculina caerulea (Pasulka et al, 2017), and white limpets Lepidodrilus fucensis on hydrothermal crusts consisting mainly of amorphous silica and clays or of barite.…”