Microbial communities in dark oligotrophic volcanic ice cave ecosystems of Mt. Erebus, Antarctica

Abstract

The Earth's crust hosts a subsurface, dark, and oligotrophic biosphere that is poorly understood in terms of the energy supporting its biomass production and impact on food webs at the Earth's surface. Dark oligotrophic volcanic ecosystems (DOVEs) are good environments for investigations of life in the absence of sunlight as they are poor in organics, rich in chemical reactants and well known for chemical exchange with Earth's surface systems. Ice caves near the summit of Mt. Erebus (Antarctica) offer DOVEs in a polar alpine environment that is starved in organics and with oxygenated hydrothermal circulation in highly reducing host rock. We surveyed the microbial communities using PCR, cloning, sequencing and analysis of the small subunit (16S) ribosomal and Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (RubisCO) genes in sediment samples from three different caves, two that are completely dark and one that receives snow-filtered sunlight seasonally. The microbial communities in all three caves are composed primarily of Bacteria and fungi; Archaea were not detected. The bacterial communities from these ice caves display low phylogenetic diversity, but with a remarkable diversity of RubisCO genes including new deeply branching Form I clades, implicating the Calvin-Benson-Bassham (CBB) cycle as a pathway of CO2 fixation. The microbial communities in one of the dark caves, Warren Cave, which has a remarkably low phylogenetic diversity, were analyzed in more detail to gain a possible perspective on the energetic basis of the microbial ecosystem in the cave. Atmospheric carbon (CO2 and CO), including from volcanic emissions, likely supplies carbon and/or some of the energy requirements of chemoautotrophic microbial communities in Warren Cave and probably other Mt. Erebus ice caves. Our work casts a first glimpse at Mt. Erebus ice caves as natural laboratories for exploring carbon, energy and nutrient sources in the subsurface biosphere and the nutritional limits on life.

Wind-driven distribution of bacteria in coastal Antarctica: evidence from the Ross Sea region

“…More recent work has described the composition of microbial communities in caves near the Mt. Erebus summit using a clone library (Tebo et al 2015) and in hot soils on Tramway Ridge using 454 sequencing (Herbold et al 2014). A reanalysis of the data from Herbold et al (2014) using the methods described here identified a large number of Cyanobacteria (5.3 % of total reads) belonging to the genera Plectolyngbya, Scytonema, and Fischerella.…”

Casamino acids slow motility and stimulate surface growth in an extreme oligotroph

“…Such adaptations are important for microorganisms living on rock surfaces, which are often depleted in organic carbon, fixed nitrogen and biologically available phosphorus (Wainwright et al ., ; Barton et al ., ). Photoautotrophs inhabiting rocks exposed to sunlight can provide a source of fixed carbon to the wider microbial community, but environments that are largely isolated from photosynthetic carbon, such as marine sediments (Lever et al ., ) and caves (Barton et al ., ; Tebo et al ., ), are more usually colonized by oligotrophic and chemoautotrophic communities. Previous studies have suggested that the enhanced adhesion of cells to nutrient‐rich surfaces in marine sediments and the subsequent establishment of biofilms are important adaptations for microorganisms that would otherwise be starving in oligotrophic waters (Marshall, ).…”

Functional metagenomic selection of ribulose 1, 5‐bisphosphate carboxylase/oxygenase from uncultivated bacteria

“…Most of what is known regarding bacterial RubisCO function is derived from pure culture analyses and relatively few model enzymes. However, recent massive deoxyribonucleic acid (DNA) sequencing efforts have shown the abundant presence of diverse and novel RubisCO‐encoding genes in environmental communities of largely uncultivated bacteria and new candidate phyla, the so‐called ‘microbial dark matter’ (Wrighton et al ., 2012; submitted; Campbell et al ., ; Guo et al ., ; Castelle et al ., ; Tebo et al ., ). Although the physiological significance of these novel RubisCO enzymes is unquantified, these organisms likely have evolved significant structural and functional adaptations to allow CO 2 to be metabolized in diverse environments such as in marine surface waters, hydrothermal vents and the terrestrial subsurface (Witte et al ., ; Wrighton et al ., 2012; submitted; Böhnke and Perner, ; Castelle et al ., ).…”

“…Sequencing, cloning and activity screening of purified recombinant proteins is possible on a small scale (Böhnke and Perner, 2015). However, it is not always possible to discern physiological function by sequence-gazing alone, nor is it practical to produce and individually screen and characterize recombinant proteins from the large number of novel RubisCO-encoding genes recently observed (Wrighton et al, 2012;submitted;Campbell et al, 2013;Guo et al, 2013;Castelle et al, 2015;Tebo et al, 2015). Whereas a previous study demonstrated the feasibility of studying environmentally derived RubisCO genes in a recombinant photosynthetic host (Witte et al, 2010), a directed functional metagenomic selection approach is necessary for highthroughput retrieval of desirable new RubisCO enzymes from uncultivated organisms.…”