Metagenomic insights into an enigmatic gammaproteobacterium that is important for carbon cycling in cave ecosystems worldwide

Caves are windows into the subsurface through which we can directly evaluate the microbiological processes responsible for rock weathering and biogeochemical cycling in more expansive areas of Earth’s subsurface. However, many cave microbial communities are dominated by microorganisms from uncultivated groups with unknown genomic capabilities that cannot be resolved from marker gene surveys alone. An example of this is a genus of Gammaproteobacteria known as “wb1-P19”, which are ubiquitous and abundant in rRNA gene surveys from limestone and volcanic caves around the world. We recovered a nearly complete metagenome-assembled genome (MAG) representing a population of wb1-P19 from Lehman Caves in Great Basin National Park, Nevada, USA, and used it to identify additional MAGs representing this group from the Frasassi Caves in Italy and in publicly available databases. Although members of the wb1-P19 group have often been thought to be autotrophs that oxidize inorganic nitrogen compounds, we show that wb1-P19 are actually obligate or facultative methanotrophs capable of aerobic and anaerobic growth. Based on genomic classification, wb1-P19 are members of upland soil cluster γ (USCγ; part of the newly proposed order “ Candidatus Methyloligotrophales”), and are likely important for methane consumption and carbon cycling in caves and other subterranean ecosystems globally.