Degradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments
Open Access
- 10 June 2021
- journal article
- research article
- Published by Oxford University Press (OUP) in The ISME Journal
- Vol. 15 (12), 3480-3497
- https://doi.org/10.1038/s41396-021-01026-5
Abstract
Hydrothermal sediments contain large numbers of uncultured heterotrophic microbial lineages. Here, we amended Guaymas Basin sediments with proteins, polysaccharides, nucleic acids or lipids under different redox conditions and cultivated heterotrophic thermophiles with the genomic potential for macromolecule degradation. We reconstructed 20 metagenome-assembled genomes (MAGs) of uncultured lineages affiliating with known archaeal and bacterial phyla, including endospore-forming Bacilli and candidate phylum Marinisomatota. One Marinisomatota MAG had 35 different glycoside hydrolases often in multiple copies, seven extracellular CAZymes, six polysaccharide lyases, and multiple sugar transporters. This population has the potential to degrade a broad spectrum of polysaccharides including chitin, cellulose, pectin, alginate, chondroitin, and carrageenan. We also describe thermophiles affiliating with the genera Thermosyntropha, Thermovirga, and Kosmotoga with the capability to make a living on nucleic acids, lipids, or multiple macromolecule classes, respectively. Several populations seemed to lack extracellular enzyme machinery and thus likely scavenged oligo- or monomers (e.g., MAGs affiliating with Archaeoglobus) or metabolic products like hydrogen (e.g., MAGs affiliating with Thermodesulfobacterium or Desulforudaceae). The growth of methanogens or the production of methane was not observed in any condition, indicating that the tested macromolecules are not degraded into substrates for methanogenesis in hydrothermal sediments. We provide new insights into the niches, and genomes of microorganisms that actively degrade abundant necromass macromolecules under oxic, sulfate-reducing, and fermentative thermophilic conditions. These findings improve our understanding of the carbon flow across trophic levels and indicate how primary produced biomass sustains complex and productive ecosystems.Keywords
This publication has 110 references indexed in Scilit:
- Archaeal and bacterial diversity in an arsenic-rich shallow-sea hydrothermal system undergoing phase separationFrontiers in Microbiology, 2013
- SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell SequencingJournal of Computational Biology, 2012
- Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of VerrucomicrobiaPLOS ONE, 2012
- Microbial control over carbon cycling in soilFrontiers in Microbiology, 2012
- Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sedimentsThe ISME Journal, 2011
- Quality control and preprocessing of metagenomic datasetsBioinformatics, 2011
- PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotesBioinformatics, 2010
- A functional analysis of the pyrimidine catabolic pathway in ArabidopsisNew Phytologist, 2009
- Structure, Function, and Evolution of Bacterial ATP-Binding Cassette SystemsMicrobiology and Molecular Biology Reviews, 2008
- Diversity and Metabolism of Marine Bacteria Cultivated on Dissolved DNAApplied and Environmental Microbiology, 2007