Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Autor(en)

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, Chris Greening

Abstrakt

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.

Organisation(en)

Department für Funktionelle und Evolutionäre Ökologie, Department für Botanik und Biodiversitätsforschung

Externe Organisation(en)

Department of Microbiology, Anatomy, Physiology & Pharmacology, La Trobe University, Melbourne, VIC, Australia. S.Bay@latrobe.edu.au., Monash University, School of Chemistry, Monash University, Melbourne, VIC, Australia., Aalborg University (AAU), Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, The Arctic University of Norway, Tromsø, Norway., Department of Environment and Genetics, La Trobe University, Melbourne, VIC, Australia., Victorian Speleological Association Inc, Melbourne, VIC, Australia., School of Biological Sciences, Monash University, Melbourne, VIC, Australia. steven.chown@monash.edu., Department of Microbiology, Biomedicine Discovery Institute, Monash University, Melbourne, VIC, Australia. chris.greening@monash.edu.

Journal

Nature Communications

Band

16

Seiten

10295

ISSN

2041-1723

DOI

https://doi.org/10.1038/s41467-025-65209-w

Publikationsdatum

11-2025

Peer-reviewed

Ja

ÖFOS 2012

106022 Mikrobiologie

Schlagwörter

Link zum Portal

https://ucrisportal.univie.ac.at/de/publications/e5b41ec1-c83c-4107-a66b-ff68e0703304