Influence of Regional Oceanography and Hydrothermal Activity on Protist Diversity and Community Structure in the Okinawa Trough

Abstract

Protist diversity and biogeography in the Okinawa Trough 2 Microbial eukaryotes (protists) contribute substantially to ecological functioning in marine ecosystems, but the relative importance of factors shaping protist diversity, such as environmental selection and dispersal, remain difficult to parse. Water masses of a back-arc basin with hydrothermal activity provide a unique opportunity for studying the effects of dispersal and environmental selection on protist communities. In this study, we used metabarcoding to characterize protist communities in the Okinawa Trough, a back-arc spreading basin containing at least twenty-five active hydrothermal vent fields.Water was sampled from four depths at fourteen stations spanning the length of the Okinawa Trough, including three sites influenced by nearby hydrothermal vent sites. While significant differences in community structure reflecting water depth were present, protist communities were mostly homogeneous horizontally. Protist communities in bottom waters affected by hydrothermal activity were significantly different from communities in other bottom waters, suggesting that environmental factors can be especially important in shaping community composition under specific conditions. Amplicon sequence variants that were enriched in hydrothermally influenced bottom waters largely derived from cosmopolitan protists that were present, but rare, in other near-bottom samples, thus highlighting the importance of the rare biosphere.

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

“…The Oligohymenophorea and Spirotrichea classes were particularly enriched within Gorda vent fluids (Figures 2, 3), and species within these groups may be specially suited to thrive within the vent environment. For example, scuticociliates (a subclass within Oligohymenophorea; Table S5) have been found previously near hydrothermal vent sites (28, 32), and in addition to their heterotrophic capabilities, are known to be parasitic or to host endosymbionts (31). Ciliates found only within the vent fluid samples, such as Karyorelictea, Plagiopylea, and Euplotia , include species capable of thriving in low oxygen to suboxic environments with modified mitochondria (hydrogenosomes).…”

“…Heterotrophic nanoflagellate members of the stramenopile supergroup were overwhelmingly MArine STramenopiles (MAST, in cosmopolitan and resident populations) or Cafeteriaceae (primarily in the near vent bottom water samples) ( Figure 3); both are recognized as important bacterivores with a global distribution and often found in mesopelagic and deep sea surveys (35)(36)(37). MAST have also been found at higher relative sequence abundances within the Mariana Arc vent ecosystem and hydrothermally influenced water masses within Okinawa Trough (17,28).…”

Structural Comparison of Diplonemid Communities around the Izu Peninsula, Japan

“…The protist community structures of various samples have been analyzed ( e.g. , Brisbin et al , 2020 ; Iniesto et al , 2021 ), and differences among these samples were successfully characterized. A comparison of the bulk structure of an entire protist community is important for understanding structural differences at the large-scale level.…”

Hydrothermal trace metal release and microbial metabolism in the Northeast Lau Basin of the south Pacific Ocean

“…Deep sea communities therefore may be relying on metabolic plasticity to exploit a variety of environmental conditions, enabling the occupation of both hydrothermal and non-hydrothermal influenced seawater systems. Protistan groups such as ciliates, stramenopiles, dinoflagellates and radiolarians are also ubiquitous in the deep ocean, and may serve as important vectors for transferring carbon obtained from vent sites to the broader bathypelagic ocean (Olsen et al 2015;Murdock and Juniper 2019;Mars Brisbin et al 2020). However, hydrothermal populations can be genomically distinct from background communities at a fine taxonomic level, which has been observed in vent-influenced protistan communities using amplicon sequence variants (ASVs) (Mars Brisbin et al 2020;Hu et al 2021) and bacterial functional genes (Mino et al 2013(Mino et al , 2017, although this was not observed here using an OTU approach.…”

“…Protistan groups such as ciliates, stramenopiles, dinoflagellates and radiolarians are also ubiquitous in the deep ocean, and may serve as important vectors for transferring carbon obtained from vent sites to the broader bathypelagic ocean (Olsen et al 2015;Murdock and Juniper 2019;Mars Brisbin et al 2020). However, hydrothermal populations can be genomically distinct from background communities at a fine taxonomic level, which has been observed in vent-influenced protistan communities using amplicon sequence variants (ASVs) (Mars Brisbin et al 2020;Hu et al 2021) and bacterial functional genes (Mino et al 2013(Mino et al , 2017, although this was not observed here using an OTU approach. Interestingly, disconnects between the amplicon and proteomic datasets were apparent with the 16S rRNA analysis indicating cyanobacteria were one of the most relatively abundant taxa identified even in deep waters (≥ 200 m; Fig.…”