Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Sean K. Bay (), Gaofeng Ni, Rachael Lappan, Pok Man Leung, Wei Wen Wong, S. I. Ry Holland, Nadeesha Athukorala, Kalinka Sand Knudsen, Ziqi Fan, Melina Kerou, Surbhi Jain, Oliver Schmidt, Vera Eate, David A. Clarke, Thanavit Jirapanjawat, Alexander Tveit, Tim Featonby, Susan White, Nicholas White, Melodie A. McGeoch, Caitlin M. Singleton, Perran L. M. Cook, Steven L. Chown () and Chris Greening ()
Additional contact information
Sean K. Bay: Monash University, Securing Antarctica’s Environmental Future
Gaofeng Ni: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Rachael Lappan: Monash University, Securing Antarctica’s Environmental Future
Pok Man Leung: Monash University, Securing Antarctica’s Environmental Future
Wei Wen Wong: Monash University, School of Chemistry
S. I. Ry Holland: Monash University, Securing Antarctica’s Environmental Future
Nadeesha Athukorala: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Kalinka Sand Knudsen: Aalborg University, Center for Microbial Communities, Department of Chemistry and Bioscience
Ziqi Fan: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Melina Kerou: University of Vienna, Archaea Biology and Ecogenomics Unit, Department of Functional and Evolutionary Biology
Surbhi Jain: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Oliver Schmidt: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Vera Eate: Monash University, School of Chemistry
David A. Clarke: Monash University, Securing Antarctica’s Environmental Future
Thanavit Jirapanjawat: Monash University, Department of Microbiology, Biomedicine Discovery Institute
Alexander Tveit: The Arctic University of Norway, Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics
Tim Featonby: La Trobe University, Department of Environment and Genetics
Susan White: La Trobe University, Department of Environment and Genetics
Nicholas White: Victorian Speleological Association Inc
Melodie A. McGeoch: Monash University, Securing Antarctica’s Environmental Future
Caitlin M. Singleton: Aalborg University, Center for Microbial Communities, Department of Chemistry and Bioscience
Perran L. M. Cook: Monash University, School of Chemistry
Steven L. Chown: Monash University, Securing Antarctica’s Environmental Future
Chris Greening: Monash University, Securing Antarctica’s Environmental Future

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: Abstract Aerated caves receive minimal light energy, yet host diverse microbial communities and the strategies allowing them to meet energy and carbon needs remain unclear. We determined the processes and mediators of primary production in aerated limestone and basalt caves through paired metagenomic and biogeochemical profiling. Four caves were sampled, including sediments and biofilms, yielding 94 metagenomes. Based on 1458 metagenome-assembled genomes, over half of microbial cells encode enzymes to use atmospheric trace gases as energy and carbon sources. The most abundant microbes are chemosynthetic primary producers, notably the gammaproteobacterial methanotrophic order Ca. Methylocavales and two uncultivated actinobacterial genera predicted to grow on atmospheric hydrogen, carbon dioxide, and carbon monoxide. Biogeochemical and isotopic measurements confirmed that these gases are rapidly consumed at rates likely sustaining a substantial fraction of the community and potentially driving primary production. Conventional chemolithoautotrophs, using ammonium and sulfide, are also enriched and active. Altogether, these results indicate that caves are unique in microbial biodiversity and the biogeochemical processes sustaining them. Consumption of atmospheric trace gases likely has a dual role in caves, providing energy for microbial survival and potentially supporting chemosynthetic growth, thereby introducing organic carbon. This process, defined as ‘aerotrophy’, operates alongside organic and inorganic inputs.

Date: 2025
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DOI: 10.1038/s41467-025-65209-w

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