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Abstract
Antarctic desert soil ecosystems are predominately comprised of prokaryotes, which have developed unique ecological functions to cope with the extreme environmental conditions experienced in Antarctica. While Antarctic soils have exhibited diverse microbial community structures, including the presence of rare bacterial lineages, the ecological functions or genomic capacities of the microbial dark matter in this environment has remained largely unexplored.
Mitchell Peninsula and Robinson Ridge are polar desert sites located in the Windmill Islands, East Antarctica, which are very low in carbon and nitrogen. Here, PCR amplicon 454 pyrosequencing targeting the bacterial SSU rRNA genes revealed both sites to encompass a microbial community “hotspot” comprised of a high relative abundance of candidate phyla WPS-2 (9.3%) and AD3 (5.1%), as well as uncultured Chloroflexi and Actinobacteria. In addition, the abundance of Cyanobacteria, the primary carbon and nitrogen fixer in many environments, including Antarctica, was extremely low (average 0.35%).
Shotgun metagenomics and differential coverage binning was used to recover 23 draft genomes from Robinson Ridge, including for the first time, two candidate division WPS-2 and three AD3 draft genomes. While Cyanobacteria abundance was confirmed to be low, metagenomic analysis revealed that 45% of the draft genomes recovered were carrying a novel type IE RuBisCO, indicative of carbon fixation. With no bacterial chlorophyll or rhodopsin identified, a dark carbon fixation process reliant on the oxidation of atmospheric H2 and CO was discovered. This process occurs through the use of the novel 1E RuBisCO, as well as specialised high affinity type 1h/5 [NiFe]-hydrogenases and carbon monoxide dehydrogenases, all of which were also widely distributed in the Robinson Ridge metagenome. In contrast to the major carbon acquisition pathway identified, no nitrogen fixation genes were present, yet denitrification capacity was widely detected in the draft genomes. As denitrification would lead to the loss of nitrogen from the ecosystem, the balance of nitrogen in Windmill Islands region needs further investigation.
An inconsistency in the classification of WPS-2 was identified across the major SSU rRNA gene databases. WPS-2 in Greengenes was comprised of two bacterial phyla: WPS-2 and SHA-109, while WPS-2 in RDP was actually sequences from Planctomycetes. Phylogenetic analysis revealed WPS-2 to be comprised of two sub-clusters that has a close relationship to phylum Chloroflexi. I propose these sub-clusters to be composed of either facultative autotrophs (sub-cluster I) or obligative heterotrophs (sub-cluster II). Genomic inference and fluorescence in situ hybridisation showed in Antarctic soils, WPS-2 bacteria exist as small diderm cocci, with diameters ranging between 0.6-1.2 m.
Here, I propose that the microbial community in the extremely carbon-limited soils of Mitchell Peninsula and Robinson Ridge have developed a unique dark carbon fixation process based on the use of a highly dependable fuel source: atmospheric gases. Using trace H2 and CO as energy sources, provides a huge advantage for microbes surviving in the extreme polar desert environments of East Antarctica. I believe that in this ecosystem, atmospheric carbon fixation, which is distinct from phototrophy or geothermal chemotrophy is actually a novel primary production strategy supporting life in this harsh environment. Gas chromatography and isotope labelling experiments are required to confirm this hypothesis and confirmation will change our understanding on the nutritional limits required to sustain life.