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

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 CO2-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 CO2-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

The Family Streptomycetaceae

The family Streptomycetaceae comprises the genera Streptomyces, Kitasatospora, and Streptacidiphilus that are very difficult to differentiate both with genotypic and phenotypic characteristics. A separate generic status for Kitasatospora and Streptacidiphilus is questionable. Members of the family can be characterized as non-acid-alcohol-fast actinomycetes that generate most often an extensively branched substrate mycelium that rarely fragments. At maturity, the aerial mycelium forms chains of few to many spores. A large variety of pigments is produced, responsible for the color of the substrate and aerial mycelium. The organisms are chemoorganotrophic with an oxidative type of metabolism and grow within different pH ranges. Streptomyces are notable for their complex developmental cycle and production of bioactive secondary metabolites, producing more than a third of commercially available antibiotics. Antibacterial, antifungal, antiparasitic, and immunosuppressant compounds have been identified as products of Streptomyces secondary metabolism. Streptomyces can be distinguished from other filamentous actinomycetes on the basis of morphological characteristics, in particular by vegetative mycelium, aerial mycelium, and arthrospores. The genus comprises at the time of writing more than 600 species with validated names. 16S rRNA gene sequence-based analysis for species delineation within the Streptomycetaceae is of limited value. The variations within the 16S rRNA genes—even in the variable regions—are too small to resolve problems of species differentiation and to establish a taxonomic structure within the genus. Comprehensive comparative studies including protein-coding gene sequences with higher phylogenetic resolution and genome-based studies are needed to clarify the species delineation within the Streptomycetaceae