Contribution of soil bacteria to the atmosphere across biomes.

The dispersion of microorganisms through the atmosphere is a continual and essential process that underpins biogeography and ecosystem development and function. Despite the ubiquity of atmospheric microorganisms globally, specific knowledge of the determinants of atmospheric microbial diversity at any given location remains unresolved. Here we describe bacterial diversity in the atmospheric boundary layer and underlying soil at twelve globally distributed locations encompassing all major biomes, and characterise the contribution of local and distant soils to the observed atmospheric community. Across biomes the diversity of bacteria in the atmosphere was negatively correlated with mean annual precipitation but positively correlated to mean annual temperature. We identified distinct non-randomly assembled atmosphere and soil communities from each location, and some broad trends persisted across biomes including the enrichment of desiccation and UV tolerant taxa in the atmospheric community. Source tracking revealed that local soils were more influential than distant soil sources in determining observed diversity in the atmosphere, with more emissive semi-arid and arid biomes contributing most to signatures from distant soil. Our findings highlight complexities in the atmospheric microbiota that are relevant to understanding regional and global ecosystem connectivity.

Corrigendum: Subsurface Microbial Habitats in an Extreme Desert Mars-Analog Environment.

[This corrects the article DOI: 10.3389/fmicb.2019.00069.].

Subsurface Microbial Habitats in an Extreme Desert Mars-Analog Environment.

Sediments in the hyper-arid core of the Atacama Desert are a terrestrial analog to Mars regolith. Understanding the distribution and drivers of microbial life in the sediment may give critical clues on how to search for biosignatures on Mars. Here, we identify the spatial distribution of highly specialized bacterial communities in previously unexplored depth horizons of subsurface sediments to a depth of 800 mm. We deployed an autonomous rover in a mission-relevant Martian drilling scenario with manual sample validation. Subsurface communities were delineated by depth related to sediment moisture. Geochemical analysis indicated soluble salts and minerology that influenced water bio-availability, particularly in deeper sediments. Colonization was also patchy and uncolonized sediment was associated with indicators of extreme osmotic challenge. The study identifies linkage between biocomplexity, moisture and geochemistry in Mars-like sediments at the limit of habitability and demonstrates feasibility of the rover-mounted drill for future Mars sample recovery.

Global Diversity of Desert Hypolithic Cyanobacteria.

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.

Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert.

The Namib Desert is considered the oldest desert in the world and hyperarid for the last 5 million years. However, the environmental buffering provided by quartz and other translucent rocks supports extensive hypolithic microbial communities. In this study, open soil and hypolithic microbial communities have been investigated along an East-West transect characterized by an inverse fog-rainfall gradient. Multivariate analysis showed that structurally different microbial communities occur in soil and in hypolithic zones. Using variation partitioning, we found that hypolithic communities exhibited a fog-related distribution as indicated by the significant East-West clustering. Sodium content was also an important environmental factor affecting the composition of both soil and hypolithic microbial communities. Finally, although null models for patterns in microbial communities were not supported by experimental data, the amount of unexplained variation (68-97 %) suggests that stochastic processes also play a role in the assembly of such communities in the Namib Desert.

Hypolithic microbial communities: between a rock and a hard place.

Drylands are the largest terrestrial biome on Earth and a ubiquitous feature is desert pavement terrain, comprising rocks embedded in the mineral soil surface. Quartz and other translucent rocks are common and microbial communities termed hypoliths develop as biofilms on their ventral surfaces. In extreme deserts these represent major concentrations of biomass, and are emerging as key to geobiological processes and soil stabilization. These highly specialized communities are dominated by cyanobacteria that support diverse heterotrophic assemblages. Here we identify global-scale trends in the ecology of hypoliths that are strongly related to climate, particularly with regard to shifts in cyanobacterial assemblages. A synthesis of available data revealed a linear trend for colonization with regard to climate, and we suggest potential application for hypoliths as 'biomarkers' of aridity on a landscape scale. The potential to exploit the soil-stabilizing properties of hypolithic colonization in environmental engineering on dryland soils is also discussed.

Ancient origins determine global biogeography of hot and cold desert cyanobacteria.

Factors governing large-scale spatio-temporal distribution of microorganisms remain unresolved, yet are pivotal to understanding ecosystem value and function. Molecular genetic analyses have focused on the influence of niche and neutral processes in determining spatial patterns without considering the temporal scale. Here, we use temporal phylogenetic analysis calibrated using microfossil data for a globally sampled desert cyanobacterium, Chroococcidiopsis, to investigate spatio-temporal patterns in microbial biogeography and evolution. Multilocus phylogenetic associations were dependent on contemporary climate with no evidence for distance-related patterns. Massively parallel pyrosequencing of environmental samples confirmed that Chroococcidiopsis variants were specific to either hot or cold deserts. Temporally scaled phylogenetic analyses showed no evidence of recent inter-regional gene flow, indicating populations have not shared common ancestry since before the formation of modern continents. These results indicate that global distribution of desert cyanobacteria has not resulted from widespread contemporary dispersal but is an ancient evolutionary legacy. This highlights the importance of considering temporal scales in microbial biogeography.

Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile.

Quartz stones are ubiquitous in deserts and are a substrate for hypoliths, microbial colonists of the underside of such stones. These hypoliths thrive where extreme temperature and moisture stress limit the occurrence of higher plant and animal life. Several studies have reported the occurrence of green hypolithic colonization dominated by cyanobacteria. Here, we describe a novel red hypolithic colonization from Yungay, at the hyper-arid core of the Atacama Desert in Chile. Comparative analysis of green and red hypoliths from this site revealed markedly different microbial community structure as revealed by 16S rRNA gene clone libraries. Green hypoliths were dominated by cyanobacteria (Chroococcidiopsis and Nostocales phylotypes), whilst the red hypolith was dominated by a taxonomically diverse group of chloroflexi. Heterotrophic phylotypes common to all hypoliths were affiliated largely to desiccation-tolerant taxa within the Actinobacteria and Deinococci. Alphaproteobacterial phylotypes that affiliated with nitrogen-fixing taxa were unique to green hypoliths, whilst Gemmatimonadetes phylotypes occurred only on red hypolithon. Other heterotrophic phyla recovered with very low frequency were assumed to represent functionally relatively unimportant taxa.

Cyanobacterial ecology across environmental gradients and spatial scales in China's hot and cold deserts.

Lithic photoautotrophic communities function as principal primary producers in the world's driest deserts, yet many aspects of their ecology remain unknown. This is particularly true for Asia, where some of the Earth's oldest and driest deserts occur. Using methods derived from plant landscape ecology, we measured the abundance and spatial distribution of cyanobacterial colonization on quartz stony pavement across environmental gradients of rainfall and temperature in the isolated Taklimakan and Qaidam Basin deserts of western China. Colonization within available habitat ranged from 0.37+/-0.16% to 12.6+/-1.8%, with cold dry desert sites exhibiting the lowest abundance. Variation between sites was most strongly correlated with moisture-related variables and was independent of substrate availability. Cyanobacterial communities were spatially aggregated at multiple scales in patterns distinct from the underlying rock pattern. Site-level differences in cyanobacterial spatial pattern (e.g. mean inter-patch distance) were linked with rainfall, whereas patchiness within sites was correlated with local geology (greater colonization frequency of large rocks) and biology (dispersal during rainfall). We suggest that cyanobacterial patchiness may also in part be self-organized - that is, an outcome of soil water-biological feedbacks. We propose that landscape ecology concepts and models linking desert vegetation, biological feedbacks and ecohydrological processes are applicable to microbial communities.

Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China's hot and cold hyperarid deserts.

Hypolithic cyanobacterial communities occur in hot and cold hyperarid environments but the physical factors determining their diversity are not well understood. Here we report hypolithic diversity and colonization of a common quartz substrate at several hyperarid locations in the ancient deserts of north-western China, that experience varying mean annual temperature, rainfall and concomitant availability of liquid water in soil. Microscopy and enrichment culture resulted only in Chroococcidiopsis morphotypes which were ubiquitous, but community phylogenetic analysis revealed considerable cyanobacterial and heterotrophic bacterial diversity. Species Richness and Shannon's Diversity Index displayed a significant positive linear correlation with availability of liquid water but not temperature or rainfall alone. Several taxonomic groups occurred only in specific climatically defined locations, while for Chroococcidiopsis, Deinococcus and Phormidium location specific lineages within these genera were also evident. Multivariate analysis was used to illustrate pronounced community shifts due to liquid water availability, although these did not significantly affect the predicted functional relationships within any given assemblage in either hot or cold, wet or dry hyperarid deserts. This study clearly demonstrates that availability of liquid water, rather than temperature or rainfall per se is the key determinant of hypolithic diversity in hyperarid locations, and furthermore that functionally similar yet taxonomically distinct communities occur, characterized by the presence of taxa that are specific to defined levels of aridity.

Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert.

The occurrence of hypolithic cyanobacteria colonizing translucent stones was quantified along the aridity gradient in the Atacama Desert in Chile, from less arid areas to the hyperarid core where photosynthetic life and thus primary production reach their limits. As mean rainfall declines from 21 to