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Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes

To describe a microbe’s physiology, including its metabolism, environmental roles, and growth characteristics, it must be grown in a laboratory culture. Unfortunately, many phylogenetically novel groups have never been cultured, so their physiologies have only been inferred from genomics and environ...

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Autores principales: Lloyd, Karen G., Steen, Andrew D., Ladau, Joshua, Yin, Junqi, Crosby, Lonnie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6156271/
https://www.ncbi.nlm.nih.gov/pubmed/30273414
http://dx.doi.org/10.1128/mSystems.00055-18
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author Lloyd, Karen G.
Steen, Andrew D.
Ladau, Joshua
Yin, Junqi
Crosby, Lonnie
author_facet Lloyd, Karen G.
Steen, Andrew D.
Ladau, Joshua
Yin, Junqi
Crosby, Lonnie
author_sort Lloyd, Karen G.
collection PubMed
description To describe a microbe’s physiology, including its metabolism, environmental roles, and growth characteristics, it must be grown in a laboratory culture. Unfortunately, many phylogenetically novel groups have never been cultured, so their physiologies have only been inferred from genomics and environmental characteristics. Although the diversity, or number of different taxonomic groups, of uncultured clades has been studied well, their global abundances, or numbers of cells in any given environment, have not been assessed. We quantified the degree of similarity of 16S rRNA gene sequences from diverse environments in publicly available metagenome and metatranscriptome databases, which we show have far less of the culture bias present in primer-amplified 16S rRNA gene surveys, to those of their nearest cultured relatives. Whether normalized to scaffold read depths or not, the highest abundances of metagenomic 16S rRNA gene sequences belong to phylogenetically novel uncultured groups in seawater, freshwater, terrestrial subsurface, soil, hypersaline environments, marine sediment, hot springs, hydrothermal vents, nonhuman hosts, snow, and bioreactors (22% to 87% uncultured genera to classes and 0% to 64% uncultured phyla). The exceptions were human and human-associated environments, which were dominated by cultured genera (45% to 97%). We estimate that uncultured genera and phyla could comprise 7.3 × 10(29) (81%) and 2.2 × 10(29) (25%) of microbial cells, respectively. Uncultured phyla were overrepresented in metatranscriptomes relative to metagenomes (46% to 84% of sequences in a given environment), suggesting that they are viable. Therefore, uncultured microbes, often from deeply phylogenetically divergent groups, dominate nonhuman environments on Earth, and their undiscovered physiologies may matter for Earth systems. IMPORTANCE In the past few decades, it has become apparent that most of the microbial diversity on Earth has never been characterized in laboratory cultures. We show that these unknown microbes, sometimes called “microbial dark matter,” are numerically dominant in all major environments on Earth, with the exception of the human body, where most of the microbes have been cultured. We also estimate that about one-quarter of the population of microbial cells on Earth belong to phyla with no cultured relatives, suggesting that these never-before-studied organisms may be important for ecosystem functions. Author Video: An author video summary of this article is available.
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spelling pubmed-61562712018-09-28 Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes Lloyd, Karen G. Steen, Andrew D. Ladau, Joshua Yin, Junqi Crosby, Lonnie mSystems Research Article To describe a microbe’s physiology, including its metabolism, environmental roles, and growth characteristics, it must be grown in a laboratory culture. Unfortunately, many phylogenetically novel groups have never been cultured, so their physiologies have only been inferred from genomics and environmental characteristics. Although the diversity, or number of different taxonomic groups, of uncultured clades has been studied well, their global abundances, or numbers of cells in any given environment, have not been assessed. We quantified the degree of similarity of 16S rRNA gene sequences from diverse environments in publicly available metagenome and metatranscriptome databases, which we show have far less of the culture bias present in primer-amplified 16S rRNA gene surveys, to those of their nearest cultured relatives. Whether normalized to scaffold read depths or not, the highest abundances of metagenomic 16S rRNA gene sequences belong to phylogenetically novel uncultured groups in seawater, freshwater, terrestrial subsurface, soil, hypersaline environments, marine sediment, hot springs, hydrothermal vents, nonhuman hosts, snow, and bioreactors (22% to 87% uncultured genera to classes and 0% to 64% uncultured phyla). The exceptions were human and human-associated environments, which were dominated by cultured genera (45% to 97%). We estimate that uncultured genera and phyla could comprise 7.3 × 10(29) (81%) and 2.2 × 10(29) (25%) of microbial cells, respectively. Uncultured phyla were overrepresented in metatranscriptomes relative to metagenomes (46% to 84% of sequences in a given environment), suggesting that they are viable. Therefore, uncultured microbes, often from deeply phylogenetically divergent groups, dominate nonhuman environments on Earth, and their undiscovered physiologies may matter for Earth systems. IMPORTANCE In the past few decades, it has become apparent that most of the microbial diversity on Earth has never been characterized in laboratory cultures. We show that these unknown microbes, sometimes called “microbial dark matter,” are numerically dominant in all major environments on Earth, with the exception of the human body, where most of the microbes have been cultured. We also estimate that about one-quarter of the population of microbial cells on Earth belong to phyla with no cultured relatives, suggesting that these never-before-studied organisms may be important for ecosystem functions. Author Video: An author video summary of this article is available. American Society for Microbiology 2018-09-25 /pmc/articles/PMC6156271/ /pubmed/30273414 http://dx.doi.org/10.1128/mSystems.00055-18 Text en Copyright © 2018 Lloyd et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Lloyd, Karen G.
Steen, Andrew D.
Ladau, Joshua
Yin, Junqi
Crosby, Lonnie
Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_full Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_fullStr Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_full_unstemmed Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_short Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_sort phylogenetically novel uncultured microbial cells dominate earth microbiomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6156271/
https://www.ncbi.nlm.nih.gov/pubmed/30273414
http://dx.doi.org/10.1128/mSystems.00055-18
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