Relating prokaryotic and microeukaryotic diversity to community function and ecosystem variability at deep-sea hydrothermal vents




Murdock, Sheryl

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Despite over four decades of research on deep-sea hydrothermal vent ecosystems, major gaps remain in our understanding of these systems. Knowledge of microeukaryote diversity, abundance, and involvement in ecosystem function lags far behind that of prokaryotes, and contributions of the non-endosymbiotic microbiome in faunal assemblages to ecosystem processes and overall hydrothermal vent microbial diversity are not known. This research addresses these gaps using high-throughput sequencing of 16S/18S rRNA genes and metagenomes from vent and surrounding non-vent habitats encompassing diffuse hydrothermal fluids, plumes, deep seawater, and microbes in assemblages of the foundation tubeworm species Ridgeia piscesae. Co-occurrence/covariance is a central method used, first, between prokaryotes with known extreme habitat preferences and microeukaryotes to infer potential endemism in the latter, and then between microbes and fauna in R. piscesae assemblages to infer interspecies interactions. Microeukaryote distribution and abundance suggest potential vent endemic microeukarya are infrequently encountered, potentially in low abundance, and belong to novel lineages of Rhizaria and Stramenopila. Potential endemism is inferred for relatives of known apusomonads, excavates, and some clades of Syndiniales. R. piscesae assemblages are shown to be hotspots of microbial taxonomic richness and exhibit a robust temperature-driven distinction in assemblage composition above and below ~25°C spanning micro, meio and macro size classes and microbial domains (Bacteria, Archaea, and micro-Eukarya). Likely interacting faunal and microbial taxa among R. piscesae assemblages are identified as ‘core communities’, which included eight macro- and meiofaunal taxa and members of the Bacteroidetes and Epsilonbacteraeota in highT communities (>25°C) and more meiofaunal species in addition to Alpha- and Gammaproteobacteria, and Actinobacteria in lowT communities (<25°C). Core communities were used to guide metagenomic investigations of microbial functional potential. Exploratory metagenomic analysis required development of new methods to deal with compositional data. ‘Enrichment leanings’ were developed to prioritize in-depth functional comparisons between sample types, which revealed clades within core community microbes with differing functional potential between highT and lowT assemblages and between assemblages and fluids. The balance of autotrophy-heterotrophy genes and patterns of genes for different carbon, nitrogen, and sulfur-cycling processes were tested as potential metrics of community-level function but did not distinguish assemblages by highT/lowT designations. This research brings us closer to understanding hydrothermal vent ecosystem function and suggests sizeable continued discovery potential.



Microbial ecology, Deep sea, Hydrothermal vents, Microeukaryotes, Ecosystem function, DNA metabarcoding, Metagenomes