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

被引:20
作者
Ray, Angelique E. [1 ]
Zhang, Eden [1 ]
Terauds, Aleks [2 ]
Ji, Mukan [3 ]
Kong, Weidong [3 ]
Ferrari, Belinda C. [1 ]
机构
[1] Univ New South Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW, Australia
[2] Dept Environm Antarctic Conservat & Management, Australian Antarctic Div, Kingston, Tas, Australia
[3] Chinese Acad Sci, Inst Tibetan Plateau Res, Key Lab Alpine Ecol & Biodivers, Beijing, Peoples R China
基金
澳大利亚研究理事会;
关键词
carbon fixation; atmospheric chemosynthesis; trace gases; photosynthesis; environmental drivers; quantitative PCR; WINDMILL ISLANDS; DESERT ROCKS; DIVERSITY; BACTERIAL; ECOLOGY; POLAR; MICROORGANISMS; H-2; CYANOBACTERIA; SEQUENCES;
D O I
10.3389/fmicb.2020.01936
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
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 x 10(3)-1.66 x 10(9)copies/g soil;hhyL, 6.84 x 10(3)-5.07 x 10(8)copies/g soil). For the Antarctic and Arctic sites, random forest and correlation analysis against 26 measured soil physicochemical parameters revealed thatrbcL1EandhhyLgenes 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.
引用
收藏
页数:13
相关论文
共 86 条
[1]   Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes [J].
Albertsen, Mads ;
Hugenholtz, Philip ;
Skarshewski, Adam ;
Nielsen, Kare L. ;
Tyson, Gene W. ;
Nielsen, Per H. .
NATURE BIOTECHNOLOGY, 2013, 31 (06) :533-+
[2]  
Archer E., 2013, Estimate permutation pvalues for importance metrics
[3]   Phylogenetic analysis of actinobacterial populations associated with Antarctic Dry Valley mineral soils [J].
Babalola, Olubukola O. ;
Kirby, Bronwyn M. ;
Le Roes-Hill, Marilize ;
Cook, Andrew E. ;
Cary, S. Craig ;
Burton, Stephanie G. ;
Cowan, Don A. .
ENVIRONMENTAL MICROBIOLOGY, 2009, 11 (03) :566-576
[4]   Quantitative analysis of mRNA amplification by in vitro transcription [J].
Baugh, L. R. ;
Hill, A. A. ;
Brown, E. L. ;
Hunter, Craig P. .
NUCLEIC ACIDS RESEARCH, 2001, 29 (05)
[5]   Life without water: how do bacteria generate biomass in desert ecosystems? [J].
Bay, Sean ;
Ferrari, Belinda ;
Greening, Chris .
MICROBIOLOGY AUSTRALIA, 2018, 39 (01) :28-32
[6]   An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia [J].
Berney, Michael ;
Greening, Chris ;
Conrad, Ralf ;
Jacobs, William R., Jr. ;
Cook, Gregory M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (31) :11479-11484
[7]   Unique Flexibility in Energy Metabolism Allows Mycobacteria to Combat Starvation and Hypoxia [J].
Berney, Michael ;
Cook, Gregory M. .
PLOS ONE, 2010, 5 (01)
[8]   Introducing BASE: the Biomes of Australian Soil Environments soil microbial diversity database [J].
Bissett, Andrew ;
Fitzgerald, Anna ;
Meintjes, Thys ;
Mele, Pauline M. ;
Reith, Frank ;
Dennis, Paul G. ;
Breed, Martin F. ;
Brown, Belinda ;
Brown, Mark V. ;
Brugger, Joel ;
Byrne, Margaret ;
Caddy-Retalic, Stefan ;
Carmody, Bernie ;
Coates, David J. ;
Correa, Carolina ;
Ferrari, Belinda C. ;
Gupta, Vadakattu V. S. R. ;
Hamonts, Kelly ;
Haslem, Asha ;
Hugenholtz, Philip ;
Karan, Mirko ;
Koval, Jason ;
Lowe, Andrew J. ;
Macdonald, Stuart ;
McGrath, Leanne ;
Martin, David ;
Morgan, Matt ;
North, Kristin I. ;
Paungfoo-Lonhienne, Chanyarat ;
Pendall, Elise ;
Phillips, Lori ;
Pirzl, Rebecca ;
Powell, Jeff R. ;
Ragan, Mark A. ;
Schmidt, Susanne ;
Seymour, Nicole ;
Snape, Ian ;
Stephen, John R. ;
Stevens, Matthew ;
Tinning, Matt ;
Williams, Kristen ;
Yeoh, Yun Kit ;
Zammit, Carla M. ;
Young, Andrew .
GIGASCIENCE, 2016, 5
[9]  
Bottos EM., 2014, ANTARCTIC TERRESTRIA, P9, DOI DOI 10.1007/978-3-642-45213-0_2
[10]   On the rocks: the microbiology of Antarctic Dry Valley soils [J].
Cary, S. Craig ;
McDonald, Ian R. ;
Barrett, John E. ;
Cowan, Don A. .
NATURE REVIEWS MICROBIOLOGY, 2010, 8 (02) :129-138