Global Diversity of Desert Hypolithic Cyanobacteria

Abstract

Global patterns in diversity were estimated for cyanobacteria-dominated hypolithic communities that colonize ventral surfaces of quartz stones and are common in desert environments. A total of 64 hypolithic communities were recovered from deserts on every continent plus a tropical moisture sufficient location. Community diversity was estimated using a combined t-RFLP fingerprinting and high throughput sequencing approach. The t-RFLP analysis revealed desert communities were different from the single non-desert location. A striking pattern also emerged where Antarctic desert communities were clearly distinct from all other deserts. Some overlap in community similarity occurred for hot, cold and tundra deserts. A further observation was that the producer-consumer ratio displayed a significant negative correlation with growing season, such that shorter growing seasons supported communities with greater abundance of producers, and this pattern was independent of macroclimate. High-throughput sequencing of 16S rRNA and nifH genes from four representative samples validated the t-RFLP study and revealed patterns of taxonomic and putative diazotrophic diversity for desert communities from the Taklimakan Desert, Tibetan Plateau, Canadian Arctic and Antarctic. All communities were dominated by cyanobacteria and among these 21 taxa were potentially endemic to any given desert location. Some others occurred in all but the most extreme hot and polar deserts suggesting they were relatively less well adapted to environmental stress. The t-RFLP and sequencing data revealed the two most abundant cyanobacterial taxa were Phormidium in Antarctic and Tibetan deserts and Chroococcidiopsis in hot and cold deserts. The Arctic tundra displayed a more heterogenous cyanobacterial assemblage and this was attributed to the maritime-influenced sampling location. The most abundant heterotrophic taxa were ubiquitous among samples and belonged to the Acidobacteria, Actinobacteria, Bacteroidetes, and Proteobacteria. Sequencing using nitrogenase gene-specific primers revealed all putative diazotrophs were Proteobacteria of the orders Burkholderiales, Rhizobiales, and Rhodospirillales. We envisage cyanobacterial carbon input to the system is accompanied by nitrogen fixation largely from non-cyanobacterial taxa. Overall the results indicate desert hypoliths worldwide are dominated by cyanobacteria and that growing season is a useful predictor of their abundance. Differences in cyanobacterial taxa encountered may reflect their adaptation to different moisture availability regimes in polar and non-polar deserts.

Keywords: biogeography; cyanobacteria; desert; dryland; hypolith.

FIGURE 1

Non-metric multidimensional scaling plot of Bray–Curtis similarities for t-RFLP defined bacterial communities recovered from hypoliths in major deserts worldwide. Circles indicate clusters of communities at a 40% dissimilarity threshold. Colors denote macroclimate (Peel and Finlayson, 2007): Polar frost (EF) = dark blue, Polar Tundra (ET) = light blue, Cold desert (BWk) = light red, Hot desert (BWh) = dark red, Tropical savanna (Af) = green.

FIGURE 2

Plot of producer/consumer ratio (P/C) for hypolithic communities versus growing season, a metric that defines the number of days per year when photosynthesis is possible (d) (Paulsen et al., 2014). Colors denote macroclimate according (Peel and Finlayson, 2007): Polar frost (EF) = dark blue, Polar Tundra (ET) = light blue, Cold desert (BWk) = light red, Hot desert (BWh) = dark red. Locations from left to right are: McMurdo Dry Valleys, Antarctica; Libyan Desert (Sahara), Libya; Taklimakan Desert, China; Devon Island (Arctic), Canada; Baja Mexico, Mexico; Atacama Desert, Chile; Simpson Desert, Australia; Mojave Desert, USA; Death Valley, USA; Colorado Plateau, USA; Tibetan Plateau, China. Line shows linear regression fit (R² = 0.2908, p < 0.0001) and shaded area denotes 95% confidence limits.

FIGURE 3

Community composition for desert hypolithic communities based upon pyrosequencing of the 16S rRNA gene. Values indicate relative abundance for each phylum. Full identification of all OTUs is listed in Supplementary Table S2.

FIGURE 4

Venn diagram illustrating distribution of OTUs among the four locations. Taxonomic classification of 16S rRNA gene sequences was made using the Ribosomal Database Project Classifier (Wang et al., 2007). A full list of all OTUs is given in Supplementary Table S2.

FIGURE 5

Phylogenetic tree of desert hypolithic cyanobacteria based upon pyrosequencing data. Heatmap shows relative abundance of the 30 most abundant cyanobacterial phylotypes in this study for each location. The phylogenetic tree was generated via RAxML (Stamatakis, 2014) with the GTRGAMMA model. A bootstrap analysis with 100 replicates was conducted and the result was used for generating bipartition support value on the best scoring tree. Bifurcation nodes with >70% bootstrap support values were annotated with an open circle, nodes with >90% bootstrap support values were annotated with a filled circle.