Cryptic microbial communities in Antarctic deserts.

T he Antarctic Dry Valleys, situated in the Ross Sea region of Eastern Antarctica, are often referred to as one of the most extreme environments on Earth. Although this statement is subject to some argument, largely surrounding the issue of what ‘‘extreme’’ actually means, there is no arguing that the combination of macroenvironmental and microenvironmental conditions to which organisms living in the Antarctic Dry Valleys are exposed represent a severe threat to organismal survival. The combination of extreme cold and desiccation, high soil salinity, low nutrient levels, high summer UV radiation levels, and physical instability caused by strong katabatic winds all contribute to the visual appearance of a sterile environment (1–3). Despite the apparent severity of the environment, life does exist in the Antarctic Dry Valleys. The article by Pointing et al. in this issue of PNAS (4) focuses on three types of cryptic microbial communities that are widespread in this environment. These communities (see Fig. 1) all represent adaptive community responses to the extreme conditions of the polar climate. The lithic environment can provide protection against some (but not all) of these conditions: i.e., protection from wind scouring and surface mobility (5), a reduction in UV exposure (6), reduced desiccation and enhanced water availability (7), and thermal buffering (5). Mean annual temperatures are generally unchanged, unlike hot desert lithic habitats where the rock provides some protection from solar heating (8). Interestingly, Pointing et al.’s study suggests that soil salinity is a major factor in community structure (but not necessarily community survival). In desert ecosystems, even modest levels of soil salinity may be an important determinant, because water activity [aw (9)], which determines biological water availability, is reduced in the presence of soluble salts (10). The study by Pointing et al. (4) shows that Dry Valley lithic communities contain a diverse range of prokaryotes and lower eukaryotes at high biomass levels (see table 1 in ref. 4), exist in surprisingly complex assemblages, and harbor a significant number of previously unreported microbial signatures. These observations raise a number of very interesting issues. First, Pointing et al. rightly suggest that an upward revision of standing biomass (and by implication, productivity) in these Antarctic soils is probably warranted. This view is supported by an earlier study (11), albeit in the low-altitude, maritime-influenced Miers Valley, which demonstrated using ATP, lipid, and DNA quantification that standing biomass was in the range of 106 to 108 cells g 1 soil, orders of magnitude higher than determined by microscopic and culture-dependent estimates (see, for example, ref. 12). Second, the presence of these complex cryptic communities appears to strongly contradict the dogma that microbial diversity is inversely proportional to the severity of the climatic conditions (13). Pointing et al. (4) also note that open soil microbial diversity was much lower in lithic communities and lacked a photoautotrophic component. This highlights one of the key elements of such lithic communities. In a very nutrient poor (oligotrophic) environment, photoautotrophic carbon input is critical to community development. They also note that many of the phylotypes identified are putative nitrogen fixers and that these organisms are likely to be responsible for complementing the nitrogen deficiency of the Dry Valley soils. Recently, hypolithic communities in the southern low altitude Dry Valley regions have been shown to be capable of acetylene reduction, the accepted functional proxy for dinitrogen fixation. The observation that cyanobacterial Chroococcidiopsis-like phylotypes in endoliths and casmoliths and Leptolyngbia in endoliths are dominant members of the respective communities is entirely consistent with previous microscopic (7, 14) and phylogenetic observations (15). The separate clustering of phylotypic signals (see figure 2 in ref. 4) for open soils, hypoliths, and chasmoliths/endoliths is likely to reflect some fundamental difference in the factors controlling the development of the communities. It may be relevant that neither the chasmolithic nor the endolithic communities have any direct interaction with the desert pavement, and some soil-related factor may account for this degree of discrimination. It is noted, however, that the most obvious candidate, salinity (K/Na and