Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave

Abstract

Carbonate caves represent subterranean ecosystems that are largely devoid of phototrophic primary production. In semiarid and arid regions, allochthonous organic carbon inputs entering caves with vadose-zone drip water are minimal, creating highly oligotrophic conditions; however, past research indicates that carbonate speleothem surfaces in these caves support diverse, predominantly heterotrophic prokaryotic communities. The current study applied a metagenomic approach to elucidate the community structure and potential energy dynamics of microbial communities, colonizing speleothem surfaces in Kartchner Caverns, a carbonate cave in semiarid, southeastern Arizona, USA. Manual inspection of a speleothem metagenome revealed a community genetically adapted to low-nutrient conditions with indications that a nitrogen-based primary production strategy is probable, including contributions from both Archaea and Bacteria. Genes for all six known CO 2 -fixation pathways were detected in the metagenome and RuBisCo genes representative of the Calvin-Benson-Bassham cycle were over-represented in Kartchner speleothem metagenomes relative to bulk soil, rhizosphere soil and deep-ocean communities. Intriguingly, quantitative PCR found Archaea to be significantly more abundant in the cave communities than in soils above the cave. MEtaGenome ANalyzer (MEGAN) analysis of speleothem metagenome sequence reads found Thaumarchaeota to be the third most abundant phylum in the community, and identified taxonomic associations to this phylum for indicator genes representative of multiple CO 2 -fixation pathways. The results revealed that this oligotrophic subterranean environment supports a unique chemoautotrophic microbial community with potentially novel nutrient cycling strategies. These strategies may provide key insights into other ecosystems dominated by oligotrophy, including aphotic subsurface soils or aquifers and photic systems such as arid deserts.

Terrestrial filamentous fungi from Gruta do Catão (São Desidério, Bahia, Northeastern Brazil) show high levels of cellulose degradation

“…Feldhake observed that the organic matter and microbial biomass content were lower in sediments from North American caves compared to forest soils. Moreover, recent research using molecular methods showed higher values for microbial biomass on the surface than inside Kartchner Caverns, USA (Ortiz et al, 2013;Ortiz et al, 2014).…”

Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology ofNitrospiraspp.

“…This analysis showed that the RSF microbial community has relatively high proportions of chaperones and genes involved in post-translational modification and protein turnover (category O) as well as coenzyme transport and metabolism (H). These two categories have been detected to be abundant in oligotrophic ecosystems in comparison with higher nutrient availability ecosystems (Ortiz et al, 2013). The abundance of chaperones may help bacteria to deal with low nutrient availability and have been related to environmental stress tolerance (Storz and Hengge, 2011).…”

Bacterial Diversity and Composition in Oylat Cave (Turkey) with Combined Sanger/Pyrosequencing Approach

“…Caves are one of the habitable extreme habitats, and microorganisms have been determined in these ecosystems based on independent culture techniques in late 1990s such as in Nullarbor Cave, Australia (Holmes et al, 2001); Wind Cave, United States (Chelius and Moore, 2004); Niu Cave, China (Zhou et al, 2007); Altamira Cave, Italy (Portillo et al, 2009); Kartcher Caverns, United States (Ortiz et al, 2014).…”