Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation

Soil microbiomes within oligotrophic cold deserts are extraordinarily diverse. Increasingly, oligotrophic sites with low levels of phototrophic primary producers are reported, leading researchers to question their carbon and energy sources. A novel microbial carbon fixation process termed atmospheri...

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Published in:Frontiers in Microbiology
Main Authors: Angelique E. Ray, Eden Zhang, Aleks Terauds, Mukan Ji, Weidong Kong, Belinda C. Ferrari
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2020
Subjects:
Online Access:https://doi.org/10.3389/fmicb.2020.01936
https://doaj.org/article/0caa951b355b4c0684b17fbc8970ef02
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spelling ftdoajarticles:oai:doaj.org/article:0caa951b355b4c0684b17fbc8970ef02 2023-05-15T13:59:23+02:00 Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation Angelique E. Ray Eden Zhang Aleks Terauds Mukan Ji Weidong Kong Belinda C. Ferrari 2020-08-01T00:00:00Z https://doi.org/10.3389/fmicb.2020.01936 https://doaj.org/article/0caa951b355b4c0684b17fbc8970ef02 EN eng Frontiers Media S.A. https://www.frontiersin.org/article/10.3389/fmicb.2020.01936/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2020.01936 https://doaj.org/article/0caa951b355b4c0684b17fbc8970ef02 Frontiers in Microbiology, Vol 11 (2020) carbon fixation atmospheric chemosynthesis trace gases photosynthesis environmental drivers quantitative PCR Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.3389/fmicb.2020.01936 2022-12-31T01:12:35Z Soil microbiomes within oligotrophic cold deserts are extraordinarily diverse. Increasingly, oligotrophic sites with low levels of phototrophic primary producers are reported, leading researchers to question their carbon and energy sources. A novel microbial carbon fixation process termed atmospheric chemosynthesis recently filled this gap as it was shown to be supporting primary production at two Eastern Antarctic deserts. Atmospheric chemosynthesis uses energy liberated from the oxidation of atmospheric hydrogen to drive the Calvin-Benson-Bassham (CBB) cycle through a new chemotrophic form of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), designated IE. Here, we propose that the genetic determinants of this process; RuBisCO type IE (rbcL1E) and high affinity group 1h-[NiFe]-hydrogenase (hhyL) are widespread across cold desert soils and that this process is linked to dry and nutrient-poor environments. We used quantitative PCR (qPCR) to quantify these genes in 122 soil microbiomes across the three poles; spanning the Tibetan Plateau, 10 Antarctic and three high Arctic sites. Both genes were ubiquitous, being present at variable abundances in all 122 soils examined (rbcL1E, 6.25 × 103–1.66 × 109 copies/g soil; hhyL, 6.84 × 103–5.07 × 108 copies/g soil). For the Antarctic and Arctic sites, random forest and correlation analysis against 26 measured soil physicochemical parameters revealed that rbcL1E and hhyL genes were associated with lower soil moisture, carbon and nitrogen content. While further studies are required to quantify the rates of trace gas carbon fixation and the organisms involved, we highlight the global potential of desert soil microbiomes to be supported by this new minimalistic mode of carbon fixation, particularly throughout dry oligotrophic environments, which encompass more than 35% of the Earth’s surface. Article in Journal/Newspaper Antarc* Antarctic Arctic Directory of Open Access Journals: DOAJ Articles Antarctic Arctic Calvin ENVELOPE(165.100,165.100,-71.283,-71.283) The Antarctic Frontiers in Microbiology 11
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic carbon fixation
atmospheric chemosynthesis
trace gases
photosynthesis
environmental drivers
quantitative PCR
Microbiology
QR1-502
spellingShingle carbon fixation
atmospheric chemosynthesis
trace gases
photosynthesis
environmental drivers
quantitative PCR
Microbiology
QR1-502
Angelique E. Ray
Eden Zhang
Aleks Terauds
Mukan Ji
Weidong Kong
Belinda C. Ferrari
Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
topic_facet carbon fixation
atmospheric chemosynthesis
trace gases
photosynthesis
environmental drivers
quantitative PCR
Microbiology
QR1-502
description Soil microbiomes within oligotrophic cold deserts are extraordinarily diverse. Increasingly, oligotrophic sites with low levels of phototrophic primary producers are reported, leading researchers to question their carbon and energy sources. A novel microbial carbon fixation process termed atmospheric chemosynthesis recently filled this gap as it was shown to be supporting primary production at two Eastern Antarctic deserts. Atmospheric chemosynthesis uses energy liberated from the oxidation of atmospheric hydrogen to drive the Calvin-Benson-Bassham (CBB) cycle through a new chemotrophic form of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), designated IE. Here, we propose that the genetic determinants of this process; RuBisCO type IE (rbcL1E) and high affinity group 1h-[NiFe]-hydrogenase (hhyL) are widespread across cold desert soils and that this process is linked to dry and nutrient-poor environments. We used quantitative PCR (qPCR) to quantify these genes in 122 soil microbiomes across the three poles; spanning the Tibetan Plateau, 10 Antarctic and three high Arctic sites. Both genes were ubiquitous, being present at variable abundances in all 122 soils examined (rbcL1E, 6.25 × 103–1.66 × 109 copies/g soil; hhyL, 6.84 × 103–5.07 × 108 copies/g soil). For the Antarctic and Arctic sites, random forest and correlation analysis against 26 measured soil physicochemical parameters revealed that rbcL1E and hhyL genes were associated with lower soil moisture, carbon and nitrogen content. While further studies are required to quantify the rates of trace gas carbon fixation and the organisms involved, we highlight the global potential of desert soil microbiomes to be supported by this new minimalistic mode of carbon fixation, particularly throughout dry oligotrophic environments, which encompass more than 35% of the Earth’s surface.
format Article in Journal/Newspaper
author Angelique E. Ray
Eden Zhang
Aleks Terauds
Mukan Ji
Weidong Kong
Belinda C. Ferrari
author_facet Angelique E. Ray
Eden Zhang
Aleks Terauds
Mukan Ji
Weidong Kong
Belinda C. Ferrari
author_sort Angelique E. Ray
title Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
title_short Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
title_full Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
title_fullStr Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
title_full_unstemmed Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation
title_sort soil microbiomes with the genetic capacity for atmospheric chemosynthesis are widespread across the poles and are associated with moisture, carbon, and nitrogen limitation
publisher Frontiers Media S.A.
publishDate 2020
url https://doi.org/10.3389/fmicb.2020.01936
https://doaj.org/article/0caa951b355b4c0684b17fbc8970ef02
long_lat ENVELOPE(165.100,165.100,-71.283,-71.283)
geographic Antarctic
Arctic
Calvin
The Antarctic
geographic_facet Antarctic
Arctic
Calvin
The Antarctic
genre Antarc*
Antarctic
Arctic
genre_facet Antarc*
Antarctic
Arctic
op_source Frontiers in Microbiology, Vol 11 (2020)
op_relation https://www.frontiersin.org/article/10.3389/fmicb.2020.01936/full
https://doaj.org/toc/1664-302X
1664-302X
doi:10.3389/fmicb.2020.01936
https://doaj.org/article/0caa951b355b4c0684b17fbc8970ef02
op_doi https://doi.org/10.3389/fmicb.2020.01936
container_title Frontiers in Microbiology
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