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,...

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Autores principales:	Jordan T. Bird, Eric D. Tague, Laura Zinke, Jenna M. Schmidt, Andrew D. Steen, Brandi Reese, Ian P. G. Marshall, Gordon Webster, Andrew Weightman, Hector F. Castro, Shawn R. Campagna, Karen G. Lloyd
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	deep subsurface enzyme assays low energy marine sediments metabolomics metatranscriptomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d423e7abca1c4ab1a265d684576e4603
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spelling	oai:doaj.org-article:d423e7abca1c4ab1a265d684576e46032021-11-15T15:55:26ZUncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments10.1128/mBio.02376-182150-7511https://doaj.org/article/d423e7abca1c4ab1a265d684576e46032019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02376-18https://doaj.org/toc/2150-7511ABSTRACT 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.Jordan T. BirdEric D. TagueLaura ZinkeJenna M. SchmidtAndrew D. SteenBrandi ReeseIan P. G. MarshallGordon WebsterAndrew WeightmanHector F. CastroShawn R. CampagnaKaren G. LloydAmerican Society for Microbiologyarticledeep subsurfaceenzyme assayslow energymarine sedimentsmetabolomicsmetatranscriptomicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	deep subsurface enzyme assays low energy marine sediments metabolomics metatranscriptomics Microbiology QR1-502
spellingShingle	deep subsurface enzyme assays low energy marine sediments metabolomics metatranscriptomics Microbiology QR1-502 Jordan T. Bird Eric D. Tague Laura Zinke Jenna M. Schmidt Andrew D. Steen Brandi Reese Ian P. G. Marshall Gordon Webster Andrew Weightman Hector F. Castro Shawn R. Campagna Karen G. Lloyd Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
description	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.
format	article
author	Jordan T. Bird Eric D. Tague Laura Zinke Jenna M. Schmidt Andrew D. Steen Brandi Reese Ian P. G. Marshall Gordon Webster Andrew Weightman Hector F. Castro Shawn R. Campagna Karen G. Lloyd
author_facet	Jordan T. Bird Eric D. Tague Laura Zinke Jenna M. Schmidt Andrew D. Steen Brandi Reese Ian P. G. Marshall Gordon Webster Andrew Weightman Hector F. Castro Shawn R. Campagna Karen G. Lloyd
author_sort	Jordan T. Bird
title	Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
title_short	Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
title_full	Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
title_fullStr	Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
title_full_unstemmed	Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
title_sort	uncultured microbial phyla suggest mechanisms for multi-thousand-year subsistence in baltic sea sediments
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d423e7abca1c4ab1a265d684576e4603
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Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments

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