Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

DOI

  • Jordan T Bird, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Eric D Tague, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Laura Zinke, Department of Physics and Astronomy, University of Southern California, Los Angeles, California, USA
  • ,
  • Jenna M Schmidt, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Andrew D Steen, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Brandi Reese, Department of Life Sciences, Texas A&M University - Corpus Christi, Corpus Christi, TX, USA.
  • ,
  • Ian P G Marshall
  • Gordon Webster, Structural Biophysics Group, Cardiff Centre for Vision Science, Cardiff University, Wales CF24 4HQ, UK; Cardiff Institute for Tissue Engineering and Repair (CITER), Cardiff University, Wales CF24 4HQ, UK.
  • ,
  • Andrew Weightman, Structural Biophysics Group, Cardiff Centre for Vision Science, Cardiff University, Wales CF24 4HQ, UK; Cardiff Institute for Tissue Engineering and Repair (CITER), Cardiff University, Wales CF24 4HQ, UK.
  • ,
  • Hector F Castro, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Shawn R Campagna, Department of Microbiology, University of Tennessee - Knoxville, Knoxville, TN, USA.
  • ,
  • Karen G Lloyd, University of Tennessee, Knoxville, Tennessee, USA klloyd@utk.edu.

Energy-starved microbes in deep marine sediments subsist at near-zero growth for thousands of years, yet the mechanisms for their subsistence are unknown because no model strains have been cultivated from most of these groups. We investigated Baltic Sea sediments with single-cell genomics, metabolomics, metatranscriptomics, and enzyme assays to identify possible subsistence mechanisms employed by uncultured Atribacteria, Aminicenantes, Actinobacteria group OPB41, Aerophobetes, Chloroflexi, Deltaproteobacteria, Desulfatiglans, Bathyarchaeota, and Euryarchaeota marine group II lineages. Some functions appeared to be shared by multiple lineages, such as trehalose production and NAD+-consuming deacetylation, both of which have been shown to increase cellular life spans in other organisms by stabilizing proteins and nucleic acids, respectively. Other possible subsistence mechanisms differed between lineages, possibly providing them different physiological niches. Enzyme assays and transcripts suggested that Atribacteria and Actinobacteria group OPB41 catabolized sugars, whereas Aminicenantes and Atribacteria catabolized peptides. Metabolite and transcript data suggested that Atribacteria utilized allantoin, possibly as an energetic substrate or chemical protectant, and also possessed energy-efficient sodium pumps. Atribacteria single-cell amplified genomes (SAGs) recruited transcripts for full pathways for the production of all 20 canonical amino acids, and the gene for amino acid exporter YddG was one of their most highly transcribed genes, suggesting that they may benefit from metabolic interdependence with other cells. Subsistence of uncultured phyla in deep subsurface sediments may occur through shared strategies of using chemical protectants for biomolecular stabilization, but also by differentiating into physiological niches and metabolic interdependencies.IMPORTANCE Much of life on Earth exists in a very slow-growing state, with microbes from deeply buried marine sediments representing an extreme example. These environments are like natural laboratories that have run multi-thousand-year experiments that are impossible to perform in a laboratory. We borrowed some techniques that are commonly used in laboratory experiments and applied them to these natural samples to make hypotheses about how these microbes subsist for so long at low activity. We found that some methods for stabilizing proteins and nucleic acids might be used by many members of the community. We also found evidence for niche differentiation strategies, and possibly cross-feeding, suggesting that even though they are barely growing, complex ecological interactions continue to occur over ultralong timescales.

Original languageEnglish
Article numbere02376-18
JournalmBio
Volume10
Issue2
Number of pages15
ISSN2150-7511
DOIs
Publication statusPublished - 16 Apr 2019

Bibliographical note

Copyright © 2019 Bird et al.

    Research areas

  • Deep subsurface, Enzyme assays, Low energy, Marine sediments, Metabolomics, Metatranscriptomics, Single-cell genomics, Subsistence

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