Evidence for successional development in Antarctic hypolithic bacterial communities

Abstract

Hypoliths (cryptic microbial assemblages that develop on the undersides of translucent rocks) are significant contributors to regional C and N budgets in both hot and cold deserts. Previous studies in the Dry Valleys of Eastern Antarctica have reported three morphologically distinct hypolithic community types: cyanobacteria dominated (type I), fungus dominated (type II) and moss dominated (type III). Here we present terminal-restriction fragment length polymorphism analyses to elucidate the bacterial community structure in hypolithons and the surrounding soils. We show clear and robust distinction in bacterial composition between bulk surface soils and hypolithons. Moreover, the bacterial assemblages were similar in types II and III hypolithons and clearly distinct from those found in type I. Through 16S rRNA gene 454 pyrosequencing, we show that Proteobacteria dominated all three types of hypolithic communities. As expected, Cyanobacteria were more abundant in type I hypolithons, whereas Actinobacteria were relatively more abundant in types II and III hypolithons, and were the dominant group in soils. Using a probabilistic dissimilarity metric and random sampling, we demonstrate that deterministic processes are more important in shaping the structure of the bacterial community found in types II and III hypolithons. Most notably, the data presented in this study suggest that hypolithic bacterial communities establish via a successional model, with the type I hypolithons acting as the basal development state.

Microbial diversity and functional capacity in polar soils

“…Through application of metagenomic approaches (Figure 1), it is now known that most extreme environments harbour lower levels of microbial diversity (species richness and relative 1 abundance), than more 'benign' ecosystems [16,17]. This is thought to be due to the requirement for specific physiological adaptations, which allow organisms to exploit the combination of physical and biochemical stressors, but result in simplified ecosystems dominated by a relatively few taxa [18,19].In contrast to many other extremophilic biomes, cold environments appear to have a higher level of spatial heterogeneity [20][21][22]. Within cold regions, both soils and permafrost niches appear to be dominated by bacterial (mainly Proteobacterial, Actinobacterial and Acidobacterial), archaeal (mostly Euryarchaeota) and fungal (dominated by Ascomycota) lineages [7,23,24,25 ] (Table 1).…”

“…In contrast to many other extremophilic biomes, cold environments appear to have a higher level of spatial heterogeneity [20][21][22]. Within cold regions, both soils and permafrost niches appear to be dominated by bacterial (mainly Proteobacterial, Actinobacterial and Acidobacterial), archaeal (mostly Euryarchaeota) and fungal (dominated by Ascomycota) lineages [7,23,24,25 ] (Table 1).…”

Ecology and biogeochemistry of cyanobacteria in soils, permafrost, aquatic and cryptic polar habitats

“…Antarctic hypolithic communities have been surveyed in considerable detail (Smith et al 2000;Wood et al 2008b;Pointing et al 2009;Makhalanyane et al 2013a). A clone library based analysis of hypolith samples indicated that sequences with close homology to Nostocales and Oscillatoriales were dominant (Khan et al 2011).…”

“…The variability in the environmental factors, together with the less than ideal levels of nutrients required for biological activity, severely restrict microbial communities in polar environments. In the absence of other photoautotrophic clades, it is accepted that cyanobacteria are largely responsible for providing the most important ecosystem services, and that cyanobacterial autotrophy supports substantial and diverse populations of heterotrophic microorganisms (such as Actinobacteria, Proteobacteria, Firmicutes and Bacteroidetes) together with smaller numbers of organisms in higher trophic levels (Aislabie et al 2006;Babalola et al 2009;Chan et al 2012;Stomeo et al 2012;Makhalanyane et al 2013a;de los Rios et al 2014;Yung et al 2014).…”

“…Both classical and modern microbiological techniques have highlighted the presence of cyanobacteria in a wide range of terrestrial Arctic and Antarctic niches, including permafrost (Jansson and Tas¸ 2014), ice shelves Bottos et al 2008), rocks (Chan et al 2012;de los Rios et al 2014;Makhalanyane et al 2014), ponds and lakes (Taton et al 2003b;Bonilla et al 2005), glaciers and the resulting meltwater streams (Nadeau and Castenholz 2000;Jungblut et al 2005), and mineral soils (Wood et al 2008b; Lee et al 2012;Makhalanyane et al 2013a). Cyanobacteria are thought to be the primary colonizers in these niches (Vincent 2000), and are known to contribute to structural stability, moisture retention and fertility (Belnap and Gardner 1993).…”