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...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-08-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00504-20 |
| _version_ | 1818386142843633664 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T03:49:21Z |
| format | Article |
| id | doaj.art-8f1b8b263dca48bd96888a3e072644f3 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-14T03:49:21Z |
| publishDate | 2020-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-8f1b8b263dca48bd96888a3e072644f32022-12-21T23:18:15ZengAmerican Society for MicrobiologymSystems2379-50772020-08-015410.1128/mSystems.00504-20Microbial Metabolic Redundancy Is a Key Mechanism in a Sulfur-Rich Glacial EcosystemChristopher B. Trivedi0Blake W. Stamps1Graham E. Lau2Stephen E. Grasby3Alexis S. Templeton4John R. Spear5Department of Civil and Environmental Engineering, Colorado School of Mines, Golden, Colorado, USADepartment of Civil and Environmental Engineering, Colorado School of Mines, Golden, Colorado, USADepartment of Geological Sciences, University of Colorado Boulder, Boulder, Colorado, USAGeological Survey of Canada—Calgary, Natural Resources Canada, Calgary, Alberta, CanadaDepartment of Geological Sciences, University of Colorado Boulder, Boulder, Colorado, USADepartment of Civil and Environmental Engineering, Colorado School of Mines, Golden, Colorado, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSystems.00504-20MAGsfunctional redundancyglaciermetabolic redundancymetagenome-assembled genomesmicrobial communities |
| spellingShingle | 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 mSystems MAGs functional redundancy glacier metabolic redundancy metagenome-assembled genomes microbial communities |
| title | 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_short | 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 |
| topic | MAGs functional redundancy glacier metabolic redundancy metagenome-assembled genomes microbial communities |
| url | https://journals.asm.org/doi/10.1128/mSystems.00504-20 |
| work_keys_str_mv | AT christopherbtrivedi microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem AT blakewstamps microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem AT grahamelau microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem AT stephenegrasby microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem AT alexisstempleton microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem AT johnrspear microbialmetabolicredundancyisakeymechanisminasulfurrichglacialecosystem |