Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia

Abstract

Hypolithic microbes, primarily cyanobacteria, inhabit the highly specialized microhabitats under translucent rocks in extreme environments. Here we report findings from hypolithic cyanobacteria found under three types of translucent rocks (quartz, prehnite, agate) in a semiarid region of tropical Australia. We investigated the photosynthetic responses of the cyanobacterial communities to light, temperature and moisture in the laboratory, and we measured the microclimatic variables of temperature and soil moisture under rocks in the field over an annual cycle. We also used molecular techniques to explore the diversity of hypolithic cyanobacteria in this community and their phylogenetic relationships within the context of hypolithic cyanobacteria from other continents. Based on the laboratory experiments, photosynthetic activity required a minimum soil moisture of 15% (by mass). Peak photosynthetic activity occurred between approximately 8 degrees C and 42 degrees C, though some photosynthesis occurred between -1 degrees C and 51 degrees C. Maximum photosynthesis rates also occurred at light levels of approximately 150-550 micromol m(-2) s(-1). We used the field microclimatic data in conjunction with these measurements of photosynthetic efficiency to estimate the amount of time the hypolithic cyanobacteria could be photosynthetically active in the field. Based on these data, we estimated that conditions were appropriate for photosynthetic activity for approximately 942 h (approximately 75 days) during the year. The hypolithic cyanobacteria community under quartz, prehnite and agate rocks was quite diverse both within and between rock types. We identified 115 operational taxonomic units (OTUs), with each rock hosting 8-24 OTUs. A third of the cyanobacteria OTUs from northern Australia grouped with Chroococcidiopsis, a genus that has been identified from hypolithic and endolithic communities from the Gobi, Mojave, Atacama and Antarctic deserts. Several OTUs identified from northern Australia have not been reported to be associated with hypolithic communities previously.

Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale

“…Overall about 70-80% of variance remained unexplained. Certainly, this is partly due to the fact that we introduced the environmental effect using a relatively broad approximation (climate categories based upon long-term mean annual temperature and precipitation), which ignored any unmeasured local environmental drivers that may be involved in determining community structure (for example, see Tracy et al, 2010). However, given previous studies on these communities that showed hypoliths develop independently of the surrounding soil (Warren-Rhodes et al, 2006; Pointing et al, 2007Pointing et al, , 2009Tracy et al, 2010) owing to the specific microclimatic conditions of rocks, and that climate and continent were independent of spatial patterns observed, it is likely that a large amount of this variation is due to environmental (for example, see Dornelas et al, 2006;Pointing et al, 2009) and/or demographic stochasticity (sensu Hubbell, 2001 andTilman, 2004).…”

“…Our data demonstrate that patterns generally interpreted as indicative of the presence of niche partitioning and non-neutral processes (for example, convergence due to relatively homogeneous environments) vary on a global biogeographical scale (continent) and also between phototrophic and heterotrophic bacteria within a given community. Given that the commonly encountered phyla in hypolithic communities include known desiccationtolerant taxa, this implies that most populations may withstand the high level of demographic stochasticity due to the patchiness of the environment in hyperarid deserts (Pointing et al, , 2009Warren-Rhodes et al, 2007;Tracy et al, 2010). Further, they may opportunistically react to the environmental stochasticity determined by rapid and extreme changes in temperature and water availability.…”

“…We targeted the hypolithic niche, ventral surfaces of quartz rocks embedded in desert soils, as this substrate is a ubiquitous feature of arid regions (Thomas, 1997) and a relatively inert substrate that supports development of microbial communities that are distinct from surrounding soils (Pointing et al, 2009). Hypolithic communities are thought to develop as a result of marginal gains in niche favorability in terms of moisture availability and possible thermal buffering (Schlesinger et al, 2003;Warren-Rhodes et al, 2006;Tracy et al, 2010), although micro-niche variability may occur between individual rocks (Tracy et al, 2010). Several studies have indicated that hypolithic communities comprise relatively simple communities dominated by cyanobacteria, with a heterotrophic component largely represented by the Acidobacteria, Actinobacteria, Bacteriodetes and proteobacterial phyla (Schlesinger et al, 2003;Warren-Rhodes et al, 2006Pointing et al, 2007Pointing et al, , 2009Wood et al, 2008;Wong et al, 2010).…”

Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley

“…However, whereas altitudinal stratification of higher plants is driven principally by temperature, our data suggest that the principal drivers for hypolithic community stratification in Miers Valley are complex. In hot deserts, both soil water content and temperature dictate the limits of diversity (Pointing et al 2007) and metabolic activity (Tracy et al 2010) and presumably community development processes, and these are likely also the principal drivers of biological processes in cold deserts such as Miers Valley. Open Access This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.…”

“…In some hot arid deserts, hypoliths are colonized only by Chroococcidiopsis sp. (Warren-Rhodes et al 2007), whilst in others, a more diverse range of taxa have been identified (Tracy et al 2010). Polar hypolithons comprise a relatively diverse cyanobacterial assemblage comprising various Oscillatoriales, Aphanocapsa, Aphanothece, Chroococcidiopsis and Gloeocapsa morphotypes (Broady 1981(Broady , 2005Cockell and Stokes 2004).…”