Coming in from the cold: potential microbial threats from the terrestrial cryosphere

The terrestrial cryosphere includes >198,000 glaciers and three ice sheets (Pfeffer et al., 2014). The paradigm of cryospheric environments as “germless continents” (Byrd, 1938) has shifted to ecosystems (Kohshima, 1984; Hodson et al., 2008). Indeed, the terrestrial cryosphere constitutes a “forgotten biome” (Anesio and Laybourn-Parry, 2012) with microbial processes influencing the fundamental dynamics of glacial systems (Edwards et al., 2014). Nevertheless, in terms of genomic diversity, glacial environments are virtual terra incognita. Recent calculations indicate glacial ice harbors ca. 1×1029 cells worldwide, and ca. 4×1021 cells are eluted by ice melt from non-Antarctic glacial systems annually (Irvine-Fynn and Edwards, 2013). Therefore, it is clear that glacial systems are major reservoirs of microbial genomic diversity. If I adopt a “colicentric” view of microbial genomes by crudely assuming that each bacterial or archaeal cell’s genome is in the order of 4.6 × 106 base pairs in size, a microbial cell budget of a High Arctic glacier surface (Irvine-Fynn et al., 2012) reveals an aeolian import of 1.9 × 1014 bp m2 h−1 coupled with a glaciofluvial export of 4.4 × 1013 bp m2 h−1 which leads to a net storage of 3.5 × 1014 bp m2 h−1 under typical summer conditions. Yet I am only aware of published high-throughput DNA sequencing datasets from less than 30 of the 198,000 glaciers (Pfeffer et al., 2014). Temporal changes in glacial diversity are even less well studied (excepting Hell et al., 2013; Maccario et al., 2014; Stibal et al., 2014). Since most studies sequence marker genes, metagenomic, and phylogenomic coverage is sparse (excepting Simon et al., 2009; Edwards et al., 2013b), and the potential for lateral gene transfer unexplored. Therefore, while glacial systems are potentially massive repositories of genomic diversity they represent virtually unexplored sequence space. Here I will focus upon the role of glacial systems as reservoirs of genomic diversity in one particular form: the accumulation, storage and release of pathogens. While the notion that mysterious entities inimical to humanity survive in ice is almost cliché in science fiction, the hypothesis that glacial systems act as “genome recyclers” was stated a decade ago (Rogers et al., 2004; Castello and Rogers, 2005; Priscu et al., 2007) and has garnered tacit empirical support. Nonetheless, the role of glacial systems as reservoirs of pathogens of humans, other animals and plants is the most “frequently asked question” in the author’s experience of engaging with stakeholders, the general public and scientists in other fields, not to mention deskbound reviewers of risk assessments. With the caveat that cryospheric microbial associated morbidity and mortality is hitherto confined to anecdotal reports of snow algae-associated diarrhea (Fiore et al., 1997) and that there are many pressing priorities in the realm of emerging infectious diseases, it appears that changes in the