Dataset Information

Microbial eukaryotes in the suboxic chemosynthetic ecosystem of Movile Cave, Romania.

ABSTRACT: Movile Cave is a small system of partially inundated galleries in limestone settings close to the Black Sea in Southeast Romania. Isolated from the surface for 6 million years, its sulfidic, methane and ammonia-rich waters harbour unique chemosynthetic prokaryotic communities that include sulphur and ammonium-metabolizing chemolithotrophs, methanogens, methanotrophs and methylotrophs. The cave also harbours cave-dwelling invertebrates and fungi, but the diversity of other microbial eukaryotes remained completely unknown. Here, we apply an 18S rRNA gene-based metabarcoding approach to study the composition of protist communities in floating microbial mats and plankton from a well-preserved oxygen-depleted cave chamber. Our results reveal a wide protist diversity with, as dominant groups, ciliates (Alveolata), Stramenopiles, especially bicosoecids, and jakobids (Excavata). Ciliate sequences dominated both, microbial mats and plankton, followed by either Stramenopiles or excavates. Stramenopiles were more prominent in microbial mats, whereas jakobids dominated the plankton fraction of the oxygen-depleted water column. Mats cultured in the laboratory were enriched in Cercozoa. Consistent with local low oxygen levels, Movile Cave protists are most likely anaerobic or microaerophilic. Several newly detected OTU clades were very divergent from cultured species or environmental sequences in databases and represent phylogenetic novelty, notably within jakobids. Movile Cave protists likely cover a variety of ecological roles in this ecosystem including predation, parasitism, saprotrophy and possibly diverse prokaryote-protist syntrophies.

SUBMITTER: Reboul G

PROVIDER: S-EPMC6697535 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Microbial eukaryotes in the suboxic chemosynthetic ecosystem of Movile Cave, Romania.

Reboul Guillaume G Moreira David D Bertolino Paola P Hillebrand-Voiculescu Alexandra Maria AM López-García Purificación P

Environmental microbiology reports 20190426 3

Movile Cave is a small system of partially inundated galleries in limestone settings close to the Black Sea in Southeast Romania. Isolated from the surface for 6 million years, its sulfidic, methane and ammonia-rich waters harbour unique chemosynthetic prokaryotic communities that include sulphur and ammonium-metabolizing chemolithotrophs, methanogens, methanotrophs and methylotrophs. The cave also harbours cave-dwelling invertebrates and fungi, but the diversity of other microbial eukaryotes re ...[more]

PMID: 30969022

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Project description:BackgroundMovile Cave (SE Romania) is a chemoautotrophically-based ecosystem fed by hydrogen sulfide-rich groundwater serving as a primary energy source analogous to the deep-sea hydrothermal ecosystems. Our current understanding of Movile Cave microbiology has been confined to the sulfidic water and its proximity, as most studies focused on the water-floating microbial mat and planktonic accumulations likely acting as the primary production powerhouse of this unique subterranean ecosystem. By employing comprehensive genomic-resolved metagenomics, we questioned the spatial variation, chemoautotrophic abilities, ecological interactions and trophic roles of Movile Cave's microbiome thriving beyond the sulfidic-rich water.ResultsA customized bioinformatics pipeline led to the recovery of 106 high-quality metagenome-assembled genomes from 7 cave sediment metagenomes. Assemblies' taxonomy spanned 19 bacterial and three archaeal phyla with Acidobacteriota, Chloroflexota, Proteobacteria, Planctomycetota, Ca. Patescibacteria, Thermoproteota, Methylomirabilota, and Ca. Zixibacteria as prevalent phyla. Functional gene analyses predicted the presence of CO2 fixation, methanotrophy, sulfur and ammonia oxidation in the explored sediments. Species Metabolic Coupling Analysis of metagenome-scale metabolic models revealed the highest competition-cooperation interactions in the sediments collected away from the water. Simulated metabolic interactions indicated autotrophs and methanotrophs as major donors of metabolites in the sediment communities. Cross-feeding dependencies were assumed only towards 'currency' molecules and inorganic compounds (O2, PO43-, H+, Fe2+, Cu2+) in the water proximity sediment, whereas hydrogen sulfide and methanol were assumedly traded exclusively among distant gallery communities.ConclusionsThese findings suggest that the primary production potential of Movile Cave expands way beyond its hydrothermal waters, enhancing our understanding of the functioning and ecological interactions within chemolithoautotrophically-based subterranean ecosystems.

Project description:The geological role of microorganisms has been widely studied in the karst cave ecosystem. However, microbial interactions and ecological functions in such a dark, humid, and oligotrophic habitat have received far less attention, which is crucial to understanding cave biogeochemistry. Herein, microorganisms from weathered rock and sediment along the Heshang Cave depth were analyzed by random matrix theory-based network and Tax4Fun functional prediction. The results showed that although the cave microbial communities have spatial heterogeneity, differential habitats drove the community structure and diversity. Actinobacteria were predominant in weathered rock, whereas Proteobacteria dominated the sediment. The sediment communities presented significantly higher alpha diversities due to the relatively abundant nutrition from the outside by the intermittent stream. Consistently, microbial interactions in sediment were more complex, as visualized by more nodes and links. The abundant taxa presented more positive correlations with other community members in both of the two networks, indicating that they relied on promotion effects to adapt to the extreme environment. The keystones in weathered rock were mainly involved in the biodegradation of organic compounds, whereas the keystone Nitrospira in sediment contributed to carbon/nitrogen fixation. Collectively, these findings suggest that microbial interactions may lead to distinct taxonomic and functional communities in weathered rock and sediment in the subsurface Heshang Cave. IMPORTANCE In general, the constant physicochemical conditions and limited nutrient sources over long periods in the subsurface support a stable ecosystem in karst cave. Previous studies on cave microbial ecology were mostly focused on community composition, diversity, and the relationship with local environmental factors. There are still many unknowns about the microbial interactions and functions in such a dark environment with little human interference. Two representative habitats, including weathered rock and sediment in Heshang Cave, were selected to give an integrated insight into microbial interactions and potential functions. The cooccurrence network, especially the subnetwork, was used to characterize the cave microbial interactions in detail. We demonstrated that abundant taxa primarily relied on promotion effects rather than inhibition effects to survive in Heshang Cave. Keystone species may play important metabolic roles in sustaining ecological functions. Our study provides improved understanding of microbial interaction patterns and community ecological functions in the karst cave ecosystem.

Dataset Information

Microbial eukaryotes in the suboxic chemosynthetic ecosystem of Movile Cave, Romania.

Publications

Microbial eukaryotes in the suboxic chemosynthetic ecosystem of Movile Cave, Romania.

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