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

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Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments. / Bird, Jordan T; Tague, Eric D; Zinke, Laura; Schmidt, Jenna M; Steen, Andrew D; Reese, Brandi; Marshall, Ian P G; Webster, Gordon; Weightman, Andrew; Castro, Hector F; Campagna, Shawn R; Lloyd, Karen G.

In: mBio, Vol. 10, No. 2, e02376-18, 16.04.2019.

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

Harvard

Bird, JT, Tague, ED, Zinke, L, Schmidt, JM, Steen, AD, Reese, B, Marshall, IPG, Webster, G, Weightman, A, Castro, HF, Campagna, SR & Lloyd, KG 2019, 'Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments', mBio, vol. 10, no. 2, e02376-18. https://doi.org/10.1128/mBio.02376-18

APA

Bird, J. T., Tague, E. D., Zinke, L., Schmidt, J. M., Steen, A. D., Reese, B., ... Lloyd, K. G. (2019). Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments. mBio, 10(2), [e02376-18]. https://doi.org/10.1128/mBio.02376-18

CBE

Bird JT, Tague ED, Zinke L, Schmidt JM, Steen AD, Reese B, Marshall IPG, Webster G, Weightman A, Castro HF, Campagna SR, Lloyd KG. 2019. Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments. mBio. 10(2). https://doi.org/10.1128/mBio.02376-18

MLA

Vancouver

Bird JT, Tague ED, Zinke L, Schmidt JM, Steen AD, Reese B et al. Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments. mBio. 2019 Apr 16;10(2). e02376-18. https://doi.org/10.1128/mBio.02376-18

Author

Bird, Jordan T ; Tague, Eric D ; Zinke, Laura ; Schmidt, Jenna M ; Steen, Andrew D ; Reese, Brandi ; Marshall, Ian P G ; Webster, Gordon ; Weightman, Andrew ; Castro, Hector F ; Campagna, Shawn R ; Lloyd, Karen G. / Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments. In: mBio. 2019 ; Vol. 10, No. 2.

Bibtex

@article{5e37ed7f9f6e450ba8b3b01a7a9e6c02,
title = "Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments",
abstract = "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.",
keywords = "Deep subsurface, Enzyme assays, Low energy, Marine sediments, Metabolomics, Metatranscriptomics, Single-cell genomics, Subsistence",
author = "Bird, {Jordan T} and Tague, {Eric D} and Laura Zinke and Schmidt, {Jenna M} and Steen, {Andrew D} and Brandi Reese and Marshall, {Ian P G} and Gordon Webster and Andrew Weightman and Castro, {Hector F} and Campagna, {Shawn R} and Lloyd, {Karen G}",
note = "Copyright {\circledC} 2019 Bird et al.",
year = "2019",
month = "4",
day = "16",
doi = "10.1128/mBio.02376-18",
language = "English",
volume = "10",
journal = "mBio (Online)",
issn = "2150-7511",
publisher = "American Society for Microbiology",
number = "2",

}

RIS

TY - JOUR

T1 - Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments

AU - Bird, Jordan T

AU - Tague, Eric D

AU - Zinke, Laura

AU - Schmidt, Jenna M

AU - Steen, Andrew D

AU - Reese, Brandi

AU - Marshall, Ian P G

AU - Webster, Gordon

AU - Weightman, Andrew

AU - Castro, Hector F

AU - Campagna, Shawn R

AU - Lloyd, Karen G

N1 - Copyright © 2019 Bird et al.

PY - 2019/4/16

Y1 - 2019/4/16

N2 - 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.

AB - 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.

KW - Deep subsurface

KW - Enzyme assays

KW - Low energy

KW - Marine sediments

KW - Metabolomics

KW - Metatranscriptomics

KW - Single-cell genomics

KW - Subsistence

U2 - 10.1128/mBio.02376-18

DO - 10.1128/mBio.02376-18

M3 - Journal article

VL - 10

JO - mBio (Online)

JF - mBio (Online)

SN - 2150-7511

IS - 2

M1 - e02376-18

ER -