Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem

ABSTRACT Biological sulfur cycling in polar, low-temperature ecosystems is an understudied phenomenon in part due to difficulty of access and the dynamic nature of glacial environments. One such environment where sulfur cycling is known to play an important role in microbial metabolisms is located a...

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Autores principales:	Christopher B. Trivedi, Blake W. Stamps, Graham E. Lau, Stephen E. Grasby, Alexis S. Templeton, John R. Spear
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	MAGs functional redundancy glacier metabolic redundancy metagenome-assembled genomes microbial communities Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8f1b8b263dca48bd96888a3e072644f3
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spelling	oai:doaj.org-article:8f1b8b263dca48bd96888a3e072644f32021-12-02T19:47:38ZMicrobial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem10.1128/mSystems.00504-202379-5077https://doaj.org/article/8f1b8b263dca48bd96888a3e072644f32020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00504-20https://doaj.org/toc/2379-5077ABSTRACT Biological sulfur cycling in polar, low-temperature ecosystems is an understudied phenomenon in part due to difficulty of access and the dynamic nature of glacial environments. One such environment where sulfur cycling is known to play an important role in microbial metabolisms is located at Borup Fiord Pass (BFP) in the Canadian High Arctic. Here, transient springs emerge from ice near the terminus of a glacier, creating a large area of proglacial aufeis (spring-derived ice) that is often covered in bright yellow/white sulfur, sulfate, and carbonate mineral precipitates accompanied by a strong odor of hydrogen sulfide. Metagenomic sequencing of samples from multiple sites and of various sample types across the BFP glacial system produced 31 metagenome-assembled genomes (MAGs) that were queried for sulfur, nitrogen, and carbon cycling/metabolism genes. An abundance of sulfur cycling genes was widespread across the isolated MAGs and sample metagenomes taxonomically associated with the bacterial classes Alphaproteobacteria and Gammaproteobacteria and Campylobacteria (formerly the Epsilonproteobacteria). This corroborates previous research from BFP implicating Campylobacteria as the primary class responsible for sulfur oxidation; however, data reported here suggested putative sulfur oxidation by organisms in both the alphaproteobacterial and gammaproteobacterial classes that was not predicted by previous work. These findings indicate that in low-temperature, sulfur-based environments, functional redundancy may be a key mechanism that microorganisms use to enable coexistence whenever energy is limited and/or focused by redox chemistry. IMPORTANCE A unique environment at Borup Fiord Pass is characterized by a sulfur-enriched glacial ecosystem in the low-temperature Canadian High Arctic. BFP represents one of the best terrestrial analog sites for studying icy, sulfur-rich worlds outside our own, such as Europa and Mars. The site also allows investigation of sulfur-based microbial metabolisms in cold environments here on Earth. Here, we report whole-genome sequencing data that suggest that sulfur cycling metabolisms at BFP are more widely used across bacterial taxa than predicted. From our analyses, the metabolic capability of sulfur oxidation among multiple community members appears likely due to functional redundancy present in their genomes. Functional redundancy, with respect to sulfur-oxidation at the BFP sulfur-ice environment, may indicate that this dynamic ecosystem hosts microorganisms that are able to use multiple sulfur electron donors alongside other metabolic pathways, including those for carbon and nitrogen.Christopher B. TrivediBlake W. StampsGraham E. LauStephen E. GrasbyAlexis S. TempletonJohn R. SpearAmerican Society for MicrobiologyarticleMAGsfunctional redundancyglaciermetabolic redundancymetagenome-assembled genomesmicrobial communitiesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	MAGs functional redundancy glacier metabolic redundancy metagenome-assembled genomes microbial communities Microbiology QR1-502
spellingShingle	MAGs functional redundancy glacier metabolic redundancy metagenome-assembled genomes microbial communities Microbiology QR1-502 Christopher B. Trivedi Blake W. Stamps Graham E. Lau Stephen E. Grasby Alexis S. Templeton John R. Spear Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
description	ABSTRACT Biological sulfur cycling in polar, low-temperature ecosystems is an understudied phenomenon in part due to difficulty of access and the dynamic nature of glacial environments. One such environment where sulfur cycling is known to play an important role in microbial metabolisms is located at Borup Fiord Pass (BFP) in the Canadian High Arctic. Here, transient springs emerge from ice near the terminus of a glacier, creating a large area of proglacial aufeis (spring-derived ice) that is often covered in bright yellow/white sulfur, sulfate, and carbonate mineral precipitates accompanied by a strong odor of hydrogen sulfide. Metagenomic sequencing of samples from multiple sites and of various sample types across the BFP glacial system produced 31 metagenome-assembled genomes (MAGs) that were queried for sulfur, nitrogen, and carbon cycling/metabolism genes. An abundance of sulfur cycling genes was widespread across the isolated MAGs and sample metagenomes taxonomically associated with the bacterial classes Alphaproteobacteria and Gammaproteobacteria and Campylobacteria (formerly the Epsilonproteobacteria). This corroborates previous research from BFP implicating Campylobacteria as the primary class responsible for sulfur oxidation; however, data reported here suggested putative sulfur oxidation by organisms in both the alphaproteobacterial and gammaproteobacterial classes that was not predicted by previous work. These findings indicate that in low-temperature, sulfur-based environments, functional redundancy may be a key mechanism that microorganisms use to enable coexistence whenever energy is limited and/or focused by redox chemistry. IMPORTANCE A unique environment at Borup Fiord Pass is characterized by a sulfur-enriched glacial ecosystem in the low-temperature Canadian High Arctic. BFP represents one of the best terrestrial analog sites for studying icy, sulfur-rich worlds outside our own, such as Europa and Mars. The site also allows investigation of sulfur-based microbial metabolisms in cold environments here on Earth. Here, we report whole-genome sequencing data that suggest that sulfur cycling metabolisms at BFP are more widely used across bacterial taxa than predicted. From our analyses, the metabolic capability of sulfur oxidation among multiple community members appears likely due to functional redundancy present in their genomes. Functional redundancy, with respect to sulfur-oxidation at the BFP sulfur-ice environment, may indicate that this dynamic ecosystem hosts microorganisms that are able to use multiple sulfur electron donors alongside other metabolic pathways, including those for carbon and nitrogen.
format	article
author	Christopher B. Trivedi Blake W. Stamps Graham E. Lau Stephen E. Grasby Alexis S. Templeton John R. Spear
author_facet	Christopher B. Trivedi Blake W. Stamps Graham E. Lau Stephen E. Grasby Alexis S. Templeton John R. Spear
author_sort	Christopher B. Trivedi
title	Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
title_short	Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
title_full	Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
title_fullStr	Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
title_full_unstemmed	Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem
title_sort	microbial metabolic redundancy is a key mechanism in a sulfur-rich glacial ecosystem
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/8f1b8b263dca48bd96888a3e072644f3
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Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial Ecosystem

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