Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Area of Science:

• Microbiology
• Geochemistry
• Ecology

Background:

• Aerated caves harbor diverse microbial communities despite minimal light.
• The energy and carbon acquisition strategies of these microbes are largely unknown.

Purpose of the Study:

• To investigate the primary production processes and mediators in aerated limestone and basalt caves.
• To understand how microbial communities meet their energy and carbon needs in light-limited cave environments.

Main Methods:

• Paired metagenomic and biogeochemical profiling of cave sediments and biofilms.
• Analysis of 94 metagenomes and 1458 metagenome-assembled genomes.
• Biogeochemical and isotopic measurements to confirm gas consumption.

Main Results:

• Over half of microbial cells possess enzymes to utilize atmospheric trace gases (H2, CO2, CO) as energy and carbon sources.
• Chemosynthetic primary producers, including methanotrophs (Ca. Methylocavales) and hydrogen/carbon monoxide oxidizers (uncultivated actinobacteria), are abundant.
• Consumption of atmospheric gases is rapid and likely sustains a significant portion of the microbial community, driving primary production.
• Conventional chemolithoautotrophs utilizing ammonium and sulfide are also active.

Conclusions:

• Caves exhibit unique microbial biodiversity and biogeochemical processes.
• Atmospheric trace gas consumption ('aerotrophy') provides energy and carbon, supporting microbial survival and chemosynthetic growth.
• Aerotrophy plays a dual role in caves, introducing organic carbon alongside other inputs.