Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes

ABSTRACT 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 an...

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Autores principales:	Karen G. Lloyd, Andrew D. Steen, Joshua Ladau, Junqi Yin, Lonnie Crosby
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	environmental microbiology phylogeny uncultured microbes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dbc94fea74184f278bbef473c9700afe
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spelling	oai:doaj.org-article:dbc94fea74184f278bbef473c9700afe2021-12-02T18:15:43ZPhylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes10.1128/mSystems.00055-182379-5077https://doaj.org/article/dbc94fea74184f278bbef473c9700afe2018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00055-18https://doaj.org/toc/2379-5077ABSTRACT 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 × 1029 (81%) and 2.2 × 1029 (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.Karen G. LloydAndrew D. SteenJoshua LadauJunqi YinLonnie CrosbyAmerican Society for Microbiologyarticleenvironmental microbiologyphylogenyuncultured microbesMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	environmental microbiology phylogeny uncultured microbes Microbiology QR1-502
spellingShingle	environmental microbiology phylogeny uncultured microbes Microbiology QR1-502 Karen G. Lloyd Andrew D. Steen Joshua Ladau Junqi Yin Lonnie Crosby Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
description	ABSTRACT 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 × 1029 (81%) and 2.2 × 1029 (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.
format	article
author	Karen G. Lloyd Andrew D. Steen Joshua Ladau Junqi Yin Lonnie Crosby
author_facet	Karen G. Lloyd Andrew D. Steen Joshua Ladau Junqi Yin Lonnie Crosby
author_sort	Karen G. Lloyd
title	Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
title_short	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_sort	phylogenetically novel uncultured microbial cells dominate earth microbiomes
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/dbc94fea74184f278bbef473c9700afe
work_keys_str_mv	AT karenglloyd phylogeneticallynovelunculturedmicrobialcellsdominateearthmicrobiomes AT andrewdsteen phylogeneticallynovelunculturedmicrobialcellsdominateearthmicrobiomes AT joshualadau phylogeneticallynovelunculturedmicrobialcellsdominateearthmicrobiomes AT junqiyin phylogeneticallynovelunculturedmicrobialcellsdominateearthmicrobiomes AT lonniecrosby phylogeneticallynovelunculturedmicrobialcellsdominateearthmicrobiomes
_version_	1718378364922757120

Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes

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