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.

Extreme environments: microbiology leading to specialized metabolites

“…These oxygenic photosynthetic prokaryotes, which form a single taxonomic and phylogenetic group, produce a broad range of bioactive compounds including ones that show anti-microbial, anti-protozoal and anti-inflammatory activity (Micallef et al 2015;Vijayakumar and Menakha 2015). Endolithic (rock-inhabiting) cyanobacteria dominated by Chroococcidiopsis species were first reported from the Negev Desert (Potts and Friedmann 1981), but are now known to be common in desert biomes given their remarkable ability to cope with extreme aridity and solar radiation (Lacap-Bugler et al 2017). Indeed, cyanobacteria dominate hypolithic (under rock) desert communities and may be major drivers of community assembly and function (Bahl et al 2011).…”

Core bacterial community composition of a cryptoendolithic ecosystem in the Grand Staircase‐Escalante National Monument, Utah

“…Comparing these communities to other desert communities, we see that with only a few exceptions, namely the Negev Desert and the Atacama Desert (Bell, 1993;Connon, Lester, Shafaat, Obenhuber, & Ponce, 2007;Crits-Christoph et al, 2013;Friedmann, Lipkin, & Ocampo-Paus, 1967;Wierzchos et al, 2012), the microbial diversity is quite similar (Antony et al, 2012;Bell, Athey, & Sommerfeld, 1986;de la Torre et al, 2003;Friedmann, 1980;Lacap-Bugler et al, 2017).…”

“…Comparing these communities to other desert communities, we see that with only a few exceptions, namely the Negev Desert and the Atacama Desert (Bell, ; Connon, Lester, Shafaat, Obenhuber, & Ponce, ; Crits‐Christoph et al., ; Friedmann, Lipkin, & Ocampo‐Paus, ; Wierzchos et al., ), the microbial diversity is quite similar (Antony et al., ; Bell, Athey, & Sommerfeld, ; de la Torre et al., ; Friedmann, ; Lacap‐Bugler et al., ). In comparison with the community structure of local desert soils, we find that the overall structure is comparable, with Cyanobacteria and Proteobacteria numbers being higher on a relative basis (Garcia‐Pichel, Johnson, Youngkin, & Belnap, ; Garcia‐Pichel, Lopez‐Cortes, & Nubel, ; Lee et al., ).…”

“…This ecological niche provides microorganisms physical stability and protection from extreme environmental conditions in hot deserts (Archer et al., ; Friedmann & Ocampo, ; Wierzchos, de los Ríos, & Ascaso, ; Yung et al., ). Cryptoendolithic communities produce extracellular polymeric substances (EPS) under moist conditions as another survival adaptation to retain water, entrap nutrients, and reduce temperature fluctuations (Antony, Cockell, & Shouche, ; Büdel et al., ; Gorbushina & Broughton, ; Kurtz, ; Lacap‐Bugler et al., ; Omelon, Pollard, & Ferris, ). It has also been observed that cryptoendolithic biomass acts to stabilize the friable sandstone surface through the production of EPS and in some cases by filamentous cell growth (Kurtz & Cox, ), protecting the sandstone surfaces from erosional processes, resulting in diverse microscale features, such as rock visors and undercut ripples in the sandstones (Kurtz & Netoff, ).…”

How environment selects: Resilience and survival of microbial mat community within intermittent karst spring Krčić (Croatia)

“…Such cosmopolitan organisms with ability to live in the most extreme environments on Earth are usually not able to compete well with specialized organisms in species-rich communities in more moderate conditions (Friedmann & Ocampo-Friedmann, 1995). This is recognized as characteristic of primitive organisms whose survival depended on the endurance of extreme conditions, where they are dominant organism forming monospecific populations (Billi, Friedmann, Hofer, Caiola, & Ocampo-Friedmann, 2000;Friedmann & Ocampo-Friedmann, 1995;Lacap-Bugler et al, 2017). Even though other bacterial groups were very lowly represented in the mat community in this second water inflow period, we found samples to be enriched with specific populations of bacteria including Chloroflexi (nonsulfur green bacteria usually responsible for anoxygenic photosynthesis) and Acidobacteria.…”