Abstract
Modern linkages among magmatic, geochemical, and geobiological processes provide clues about the importance of thermophiles in the origin of biogeochemical cycles. The aim of this study was to identify the primary chemoautotrophs and host–virus interactions involved in microbial colonization and biogeochemical cycling at sublacustrine, vapor-dominated vents that represent the hottest measured ecosystems in Yellowstone National Park (~140 °C). Filamentous microbial communities exposed to extreme thermal and geochemical gradients were sampled using a remotely operated vehicle and subjected to random metagenome sequencing and microscopic analyses. Sulfurihydrogenibium (phylum Aquificae) was the predominant lineage (up to 84% relative abundance) detected at vents that discharged high levels of dissolved H2, H2S, and CO2. Metabolic analyses indicated carbon fixation by Sulfurihydrogenibium spp. was powered by the oxidation of reduced sulfur and H2, which provides organic carbon for heterotrophic community members. Highly variable Sulfurihydrogenibium genomes suggested the importance of intra-population diversity under extreme environmental and viral pressures. Numerous lytic viruses (primarily unclassified taxa) were associated with diverse archaea and bacteria in the vent community. Five circular dsDNA uncultivated virus genomes (UViGs) of ~40 kbp length were linked to the Sulfurihydrogenibium metagenome-assembled genome (MAG) by CRISPR spacer matches. Four UViGs contained consistent genome architecture and formed a monophyletic cluster with the recently proposed Pyrovirus genus within the Caudovirales. Sulfurihydrogenibium spp. also contained CRISPR arrays linked to plasmid DNA with genes for a novel type IV filament system and a highly expressed β-barrel porin. A diverse suite of transcribed secretion systems was consistent with direct microscopic analyses, which revealed an extensive extracellular matrix likely critical to community structure and function. We hypothesize these attributes are fundamental to the establishment and survival of microbial communities in highly turbulent, extreme-gradient environments.
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Data availability
Genomic sequence information for this investigation can be found in the NCBI database under BioProject PRJNA669531 and BioSamples SAMN16454225, SAMN16454373, SAMN16454375, SAMN16454377, and SAMN16454376. Quality-filtered short reads used for single metagenomic assemblies are available in the NCBI Sequence Read Archive as SRR12852619 (2016_B01), SRR12852620 (2016_B02_str), and SRR12852618 (2016_B02_sed). Quality-filtered short reads used for coassembled metagenomes are available in the NCBI Sequence Read Archive as SRR12852621 (2017_B01_S1) and SRR12852622 (2017_B01_S2).
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Acknowledgements
The authors appreciate support from the National Science Foundation (Subaward A101357, WHOI Project 81636100 (LJM and WPI); DEB 1950770 (WPI and MD) and EPSCoR1736255 (LJM and MWF)), the Montana Agricultural Experiment Station (MAES 911300; WPI), the National Institutes of Health IDeA Program (COBRE grant GM110732; MD), and by the US Department of Energy—Ecosystems and Networks Integrated with Genes and Molecular Assemblies (DE-AC02–05CH11231; MWF). Metagenome sequencing was performed by the Census of Deep Life (Deep Carbon Observatory). Computations were performed on the Hyalite High-Performance Computing System (MSU Information Technology). Electron microscopy and elemental analyses were performed at the Montana Nanotechnology Facility, a member of the National Nanotechnology Coordinated Infrastructure (NNCI), which is supported by the NSF (ECCS-2025391). We also appreciate significant synergistic contributions from the HD-YLake project and support for KML (NSF EAR 1514865) in sampling and data sharing efforts. We thank the Global Foundation for Ocean Exploration and Capt. Dave Lovalvo for crucial shipboard support and ROV expertise, which made it possible to sample this extreme environment. Finally, we are grateful for helpful discussions with Drs. S. Abby, R. Denise, E. Rocha, Z. Jay, M. Myers, and A. Segall. Research in Yellowstone Lake (YNP, Wyoming, USA) was conducted under permit YELL-2016/17-SCI-7018. The sample from Liberty Cap (Mammoth Hot Springs, YNP) was collected in collaboration with Dr. B. Fouke under YNP research permit to WPI (YELL-2011-SCI-5686).
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LJM and WPI designed the study. LJM, ODN, and WPI wrote the manuscript. WPI acquired grant funding to support the investigation. LJM and DBR performed metagenome binning. LJM analyzed MAGs for genomic characteristics and metabolic potential. ODN scanned metagenomes for viral content, analyzed putative viral sequence, and annotated UViGs. LJM and ODN scanned and analyzed metagenomes for CRISPR information. MD constructed phylogenomic trees from concatenated protein alignments. MD and LJM calculated predicted optimal growth temperatures and performed metagenomic subsampling. LJM constructed phylogenetic trees of SCGs and annotated plasmid DNA. WPI performed scanning electron microscopy and LJM assisted in elemental analyses. KML assisted in sampling YLake biofilms, recovered ROV data and videos, and created maps of YLake. MWF assisted in metabolic analyses. All authors reviewed and edited the manuscript.
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McKay, L.J., Nigro, O.D., Dlakić, M. et al. Sulfur cycling and host-virus interactions in Aquificales-dominated biofilms from Yellowstone’s hottest ecosystems. ISME J 16, 842–855 (2022). https://doi.org/10.1038/s41396-021-01132-4
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DOI: https://doi.org/10.1038/s41396-021-01132-4
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