Enrichment of Cryoconite Hole Anaerobes: Implications for the Subglacial Microbiome

Abstract

Glaciers have recently been recognized as ecosystems comprised of several distinct habitats: a sunlit and oxygenated glacial surface, glacial ice, and a dark, mostly anoxic glacial bed. Surface meltwaters annually flood the subglacial sediments by means of drainage channels. Glacial surfaces host aquatic microhabitats called cryoconite holes, regarded as “hot spots” of microbial abundance and activity, largely contributing to the meltwaters’ bacterial diversity. This study presents an investigation of cryoconite hole anaerobes and discusses their possible impact on subglacial microbial communities, combining 16S rRNA gene fragment amplicon sequencing and the traditional enrichment culture technique. Cryoconite hole sediment harbored bacteria belonging mainly to the Proteobacteria (21%), Bacteroidetes (16%), Actinobacteria (14%), and Planctomycetes (6%) phyla. An 8-week incubation of those sediments in Postgate C medium for sulfate reducers in airtight bottles, emulating subglacial conditions, eliminated a great majority of dominant taxa, leading to enrichment of the Firmicutes (62%), Proteobacteria (14%), and Bacteroidetes (13%), which consisted of anaerobic genera like Clostridium, Psychrosinus, Paludibacter, and Acetobacterium. Enrichment of Pseudomonas spp. also occurred, suggesting it played a role as a dominant oxygen scavenger, providing a possible scenario for anaerobic niche establishment in subglacial habitats. To our knowledge, this is the first paper to provide insight into the diversity of the anaerobic part of the cryoconite hole microbial community and its potential to contribute to matter turnover in anoxic, subglacial sites.

Rapid development of anoxic niches in supraglacial ecosystems

“…Although the most common morphology of cryoconite deposit observed in this sector of the GrIS was the classic circular, water-filled structure, the large deposits (drained and accumulated) are home to comparatively large microbial habitats, much of which are anoxic. Our results contradict the belief that cryoconite holes should generally be regarded as aerobic environments (Zdanowski et al 2016b), but support the view that the primary control on biological activity is the structure of the sediment (biocryomorphology). The degree of hydrological connectivity and consequent residence time of the cryoconite is also a strong control, first by allowing the build up of a stable community structure (Bagshaw et al 2016a(Bagshaw et al , 2016b, and second by supplying nutrients via meltwater (Hodson et al 2005b;Stibal and Tranter 2007b).…”

“…They need to respond quickly to oxygen changes in their environment, which would be highly selective for facultative anaerobes, because strictly anaerobic organisms must be able to tolerate exposure to oxygen, and strict aerobes must be able to survive sudden oxygen deprivation. Characterization of anaerobes in the Antarctic cryoconite community showed that only a small percentage were strict anaerobes (Zdanowski et al 2016b). However, vertical migration of strictly anaerobic sulphate reducers along changing oxygen profiles to prevent prolonged oxygen exposure has been described (Sass et al 2002b;Taylor, Zhulin, and Johnson 1999b), and observation of our samples under a phase contrast microscope showed an abundance of motile cells.…”

“…Novel aerobic strains (e.g., Polaromonas glacialis, Polaromonas cryoconiti) were isolated and classified from Alpine glaciers (Margesin et al 2012a(Margesin et al , 2003b(Margesin et al , 2012bMargesin, Zacke, and Schinner 2002b); aerobic and potentially anaerobic groups were identified from metagenomics snapshots (Edwards et al 2013b) in the Arctic; and bacterial diversity was studied via molecular methods in Antarctic communities (Cameron, Hodson, and Osborn 2012b;Christner, Kvitko, and Reeve 2003b). Anaerobic groups have been specifically reported in enrichments from Antarctic communities (Zdanowski et al 2016b), but studies suggest that they also exist in Arctic and alpine cryoconite (Edwards et al 2014b(Edwards et al , 2013b. To date, cryoconite holes have been primarily considered an aerobic environment, with the potential for anaerobic niches within cryoconite granules (Segawa et al 2014b;Uetake et al 2016b) and thicker sediments (Bagshaw et al, 2007;Telling et al 2012b).…”

Potential sources of bacteria colonizing the cryoconite of an Alpine glacier

“…Interestingly, we observed that, despite cryocontite holes were aerobic environments [ 24 ], anaerobic Clostridiales (phylum Firmicutes) were more abundant in cryoconite than in other samples ( S1 Fig ). Clostridiales have already been recorded in cryconite from Tyrolean Alps [ 15 ] and from Antarctica [ 55 ]. and they dominated bacteria collected in snow and dust traps on the Greenland Ice Sheet [ 56 ].…”

Cryoconite Hole Location in East-Antarctic Untersee Oasis Shapes Physical and Biological Diversity

“…In contrast to Alpine and Arctic regions the number of Antarctic CH studies is low and mostly limited to glaciers around the MDVs (e.g., Christner et al, 2003;Fountain et al, 2004Fountain et al, , 2008Porazinska et al, 2004;Fortner et al, 2005;Bagshaw et al, 2007Bagshaw et al, , 2016Foreman et al, 2007;Telling et al, 2014;Webster-Brown et al, 2015;MacDonell et al, 2016) with some geographical exceptions (e.g., Cameron et al, 2012;Hodson et al, 2013;Obbels et al, 2016;Zdanowski et al, 2017). Hence, compared to the "prime study sites" such as the MDVs, little is known about the microbial ecology in CHs from e.g., Queen Maud Land (East-Antarctica).…”