'Follow the Water': Microbial Water Acquisition in Desert Soils.

Water availability is the dominant driver of microbial community structure and function in desert soils. However, these habitats typically only receive very infrequent large-scale water inputs (e.g., from precipitation and/or run-off). In light of recent studies, the paradigm that desert soil microorganisms are largely dormant under xeric conditions is questionable. Gene expression profiling of microbial communities in desert soils suggests that many microbial taxa retain some metabolic functionality, even under severely xeric conditions. It, therefore, follows that other, less obvious sources of water may sustain the microbial cellular and community functionality in desert soil niches. Such sources include a range of precipitation and condensation processes, including rainfall, snow, dew, fog, and nocturnal distillation, all of which may vary quantitatively depending on the location and geomorphological characteristics of the desert ecosystem. Other more obscure sources of bioavailable water may include groundwater-derived water vapour, hydrated minerals, and metabolic hydro-genesis. Here, we explore the possible sources of bioavailable water in the context of microbial survival and function in xeric desert soils. With global climate change projected to have profound effects on both hot and cold deserts, we also explore the potential impacts of climate-induced changes in water availability on soil microbiomes in these extreme environments.

Understanding atmospheric intercontinental dispersal of harmful microorganisms.

The atmosphere is a major route for microbial intercontinental dispersal, including harmful microorganisms, antibiotic resistance genes, and allergens, with strong implications in ecosystem functioning and global health. Long-distance dispersal is facilitated by air movement at higher altitudes in the free troposphere and is affected by anthropogenic forcing, climate change, and by the general atmospheric circulation, mainly in the intertropical convergence zone. The survival of microorganisms during atmospheric transport and their remote invasive potential are fundamental questions, but data are scarce. Extreme atmospheric conditions represent a challenge to survival that requires specific adaptive strategies, and recovery of air samples from the high altitudes relevant to study harmful microorganisms can be challenging. In this paper, we highlight the scope of the problem, identify challenges and knowledge gaps, and offer a roadmap for improved understanding of intercontinental microbial dispersal and their outcomes. Greater understanding of long-distance dispersal requires research focus on local factors that affect emissions, coupled with conditions influencing transport and survival at high altitudes, and eventual deposition at sink locations.

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.

Microbial ecology of the atmosphere.

The atmosphere connects habitats across multiple spatial scales via airborne dispersal of microbial cells, propagules and biomolecules. Atmospheric microorganisms have been implicated in a variety of biochemical and biophysical transformations. Here, we review ecological aspects of airborne microorganisms with respect to their dispersal, activity and contribution to climatic processes. Latest studies utilizing metagenomic approaches demonstrate that airborne microbial communities exhibit pronounced biogeography, driven by a combination of biotic and abiotic factors. We quantify distributions and fluxes of microbial cells between surface habitats and the atmosphere and place special emphasis on long-range pathogen dispersal. Recent advances have established that these processes may be relevant for macroecological outcomes in terrestrial and marine habitats. We evaluate the potential biological transformation of atmospheric volatile organic compounds and other substrates by airborne microorganisms and discuss clouds as hotspots of microbial metabolic activity in the atmosphere. Furthermore, we emphasize the role of microorganisms as ice nucleating particles and their relevance for the water cycle via formation of clouds and precipitation. Finally, potential impacts of anthropogenic forcing on the natural atmospheric microbiota via emission of particulate matter, greenhouse gases and microorganisms are discussed.

Desert and anthropogenic mixing dust deposition influences microbial communities in surface waters of the western Pacific Ocean.

The western Pacific Ocean is particularly affected by dust aerosols due to the transport of desert-natural sand and industrially derived particulate matter with aerodynamic diameter < 2.5 µm (PM2.5) from continental Asia. Both oligotrophic and nutrient-sufficient surface water occurs in this region and these are speculated to support different microbial community dynamics. Here, we report evidence from four shipboard experiments in the western Pacific Ocean supplying oligotrophic and nutrient-sufficient surface waters with aerosol particles obtained from the nearby coastal mountains, to simulate dust and anthropogenic aerosol inputs in the ocean region. A sharp increase in nitrate for surface waters after addition of dust aerosols resulted in large increases in diatom abundance in oligotrophic waters, whilst in nutrient-sufficient waters the response of diatom population was reduced. The increase in organic matter provided by aerosol inputs and/or increase in phytoplankton biomass induced the growth of heterotrophic prokaryotes, such as Rhodobacteraceae and Alteromonadaceae populations, in both oligotrophic and nutrient-sufficient seawater. Anthropogenic and desert-natural dust is an important source of nitrate and organics to oceanic waters and such inputs can directly affect primary production and heterotrophic prokaryotic abundance in the ocean, implying consequences for the carbon cycle in these aerosol-affected waters.

Differential Colonization and Succession of Microbial Communities in Rock and Soil Substrates on a Maritime Antarctic Glacier Forefield.

Glacier forefields provide a unique chronosequence to assess microbial or plant colonization and ecological succession on previously uncolonized substrates. Patterns of microbial succession in soils of alpine and subpolar glacier forefields are well documented but those affecting high polar systems, including moraine rocks, remain largely unexplored. In this study, we examine succession patterns in pioneering bacterial, fungal and algal communities developing on moraine rocks and soil at the Hurd Glacier forefield (Livingston Island, Antarctica). Over time, changes were produced in the microbial community structure of rocks and soils (ice-free for different lengths of time), which differed between both substrates across the entire chronosequence, especially for bacteria and fungi. In addition, fungal and bacterial communities showed more compositional consistency in soils than rocks, suggesting community assembly in each niche could be controlled by processes operating at different temporal and spatial scales. Microscopy revealed a patchy distribution of epilithic and endolithic lithobionts, and increasing endolithic colonization and microbial community complexity along the chronosequence. We conclude that, within relatively short time intervals, primary succession processes at polar latitudes involve significant and distinct changes in edaphic and lithic microbial communities associated with soil development and cryptogamic colonization.

Publisher Correction: Anthropogenic impact on the atmospheric microbiome.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Air mass source determines airborne microbial diversity at the ocean-atmosphere interface of the Great Barrier Reef marine ecosystem.

The atmosphere is the least understood biome on Earth despite its critical role as a microbial transport medium. The influence of surface cover on composition of airborne microbial communities above marine systems is unclear. Here we report evidence for a dynamic microbial presence at the ocean-atmosphere interface of a major marine ecosystem, the Great Barrier Reef, and identify that recent air mass trajectory over an oceanic or continental surface associated with observed shifts in airborne bacterial and fungal diversity. Relative abundance of shared taxa between air and coral microbiomes varied between 2.2 and 8.8% and included those identified as part of the core coral microbiome. We propose that this variable source of atmospheric inputs may in part contribute to the diverse and transient nature of the coral microbiome.

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

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

Airborne microbial transport limitation to isolated Antarctic soil habitats.

Dispersal is a critical yet poorly understood factor underlying macroecological patterns in microbial communities1. Airborne microbial transport is assumed to occupy a central role in determining dispersal outcomes2,3, and extra-range dispersal has important implications for predicting ecosystem resilience and response to environmental change4. One of the most pertinent biomes in this regard is Antarctica, given its geographic isolation and vulnerability to climate change and human disturbance5. Here, we report microbial diversity in near-ground and high-altitude air above the largest ice-free Antarctic habitat, as well as that of underlying soil microbial communities. We found that persistent local airborne inputs were unable to fully explain Antarctic soil community assembly. Comparison with airborne microbial diversity from high-altitude and non-polar sources suggests that strong selection occurs during long-range atmospheric transport. The influence of selection during airborne transit and at sink locations varied between microbial phyla. Overall, the communities from this isolated Antarctic ecosystem displayed limited connectivity to the non-polar microbial pool, and alternative sources of recruitment are necessary to fully explain extant soil diversity. Our findings provide critical insights into the role of airborne transport limitation in determining microbial biogeographic patterns.

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.

Biotic interactions are an unexpected yet critical control on the complexity of an abiotically driven polar ecosystem.

Abiotic and biotic factors control ecosystem biodiversity, but their relative contributions remain unclear. The ultraoligotrophic ecosystem of the Antarctic Dry Valleys, a simple yet highly heterogeneous ecosystem, is a natural laboratory well-suited for resolving the abiotic and biotic controls of community structure. We undertook a multidisciplinary investigation to capture ecologically relevant biotic and abiotic attributes of more than 500 sites in the Dry Valleys, encompassing observed landscape heterogeneities across more than 200 km2. Using richness of autotrophic and heterotrophic taxa as a proxy for functional complexity, we linked measured variables in a parsimonious yet comprehensive structural equation model that explained significant variations in biological complexity and identified landscape-scale and fine-scale abiotic factors as the primary drivers of diversity. However, the inclusion of linkages among functional groups was essential for constructing the best-fitting model. Our findings support the notion that biotic interactions make crucial contributions even in an extremely simple ecosystem.

Stochastic and Deterministic Effects of a Moisture Gradient on Soil Microbial Communities in the McMurdo Dry Valleys of Antarctica.

Antarctic soil supports surface microbial communities that are dependent on ephemeral moisture. Understanding the response to availability of this resource is essential to predicting how the system will respond to climate change. The McMurdo Dry Valleys are the largest ice-free soil region in Antarctica. They are a hyper-arid polar desert with extremely limited moisture availability. Microbial colonization dominates this ecosystem but surprisingly little is known about how communities respond to changing moisture regimes. We utilized the natural model system provided by transiently wetted soil at lake margins in the Dry Valleys to interrogate microbial responses along a well-defined contiguous moisture gradient and disentangle responses between and within phyla. We identified a striking non-linear response among bacteria where at low moisture levels small changes resulted in a large impact on diversity. At higher moister levels community responses were less pronounced, resulting in diversity asymptotes. We postulate that whilst the main drivers of observed community diversity were deterministic, a switch in the major influence occurred from abiotic factors at low moisture levels to biotic interactions at higher moisture. Response between and within phyla was markedly different, highlighting the importance of taxonomic resolution in community analysis. Furthermore, we resolved apparent stochasticity at high taxonomic ranks as the result of deterministic interactions taking place at finer taxonomic and spatial scales. Overall the findings provide new insight on the response to moisture and this will be useful in advancing understanding of potential ecosystem responses in the threatened McMurdo Dry Valleys system.

Characterization and Risk Assessment of Atmospheric PM2.5 and PM10 Particulate-Bound PAHs and NPAHs in Rwanda, Central-East Africa.

Exposure to airborne particulates is estimated as the largest cause of premature human mortality worldwide and is of particular concern in sub-Saharan Africa where emissions are high and data are lacking. Particulate matter (PM) contains several toxic organic species including polycyclic aromatic hydrocarbons (PAHs) and nitrated PAHs (NPAHs). This study provides the first characterization and source identification for PM10- and PM2.5-bound PAHs and NPAHs in sub-Saharan Africa during a three-month period that spanned dry and wet seasons at three locations in Rwanda. The 24-h mean PM2.5 and PM10 concentrations were significantly higher in the dry than the wet season. PAH and NPAH concentrations at the urban roadside site were significantly higher than the urban background and rural site. Source identification using diagnostic ratio analysis and principal component analysis (PCA) revealed diesel and gasoline-powered vehicles at the urban location and wood burning at the rural location as the major sources of PAHs and NPAHs. Our analysis demonstrates that PM concentrations and lifetime cancer risks resulting from inhalation exposure to PM-bound PAHs and NPAHs exceed World Health Organization safe limits. This study provides clear evidence that an immediate development of emission control measures is required.

Microbial Biomarker Transition in High-Altitude Sinter Mounds From El Tatio (Chile) Through Different Stages of Hydrothermal Activity.

Geothermal springs support microbial communities at elevated temperatures in an ecosystem with high preservation potential that makes them interesting analogs for early evolution of the biogeosphere. The El Tatio geysers field in the Atacama Desert has astrobiological relevance due to the unique occurrence of geothermal features with steep hydrothermal gradients in an otherwise high altitude, hyper-arid environment. We present here results of our multidisciplinary field and molecular study of biogeochemical evidence for habitability and preservation in silica sinter at El Tatio. We sampled three morphologically similar geyser mounds characterized by differences in water activity (i.e., episodic liquid water, steam, and inactive geyser lacking hydrothermal activity). Multiple approaches were employed to determine (past and present) biological signatures and dominant metabolism. Lipid biomarkers indicated relative abundance of thermophiles (dicarboxylic acids) and sulfate reducing bacteria (branched carboxylic acids) in the sinter collected from the liquid water mound; photosynthetic microorganisms such as cyanobacteria (alkanes and isoprenoids) in the steam sinter mound; and archaea (squalane and crocetane) as well as purple sulfur bacteria (cyclopropyl acids) in the dry sinter from the inactive geyser. The three sinter structures preserved biosignatures representative of primary (thermophilic) and secondary (including endoliths and environmental contaminants) microbial communities. Sequencing of environmental 16S rRNA genes and immuno-assays generally corroborated the lipid-based microbial identification. The multiplex immunoassays and the compound-specific isotopic analysis of carboxylic acids, alkanols, and alkanes indicated that the principal microbial pathway for carbon fixation in the three sinter mounds was through the Calvin cycle, with a relative larger contribution of the reductive acetyl-CoA pathway in the dry system. Other inferred metabolic traits varied from the liquid mound (iron and sulfur chemistry), to the steam mound (nitrogen cycle), to the dry mound (perchlorate reduction). The combined results revealed different stages of colonization that reflect differences in the lifetime of the mounds, where primary communities dominated the biosignatures preserved in sinters from the still active geysers (liquid and steam mounds), in contrast to the surviving metabolisms and microbial communities at the end of lifetime of the inactive geothermal mound.

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.

Draft Genome Sequence of Uncultured Upland Soil Cluster Gammaproteobacteria Gives Molecular Insights into High-Affinity Methanotrophy.

Aerated soils form the second largest sink for atmospheric CH4 A near-complete genome of uncultured upland soil cluster Gammaproteobacteria that oxidize CH4 at <2.5 ppmv was obtained from incubated Antarctic mineral cryosols. This first genome of high-affinity methanotrophs can help resolve the mysteries about their phylogenetic affiliation and metabolic potential.

Variations in the structure of airborne bacterial communities in Tsogt-Ovoo of Gobi desert area during dust events.

Asian dust events transport the airborne bacteria in Chinese desert regions as well as mineral particles and influence downwind area varying biological ecosystems and climate changes. However, the airborne bacterial dynamics were rarely investigated in the Gobi desert area, where dust events are highly frequent. In this study, air samplings were sequentially performed at a 2-m high above the ground at the sampling site located in desert area (Tsogt-Ovoo of Gobi desert; Mongolia 44.2304°N, 105.1700°E). During the dust event days, the bacterial cells and mineral particles increased to more than tenfold of concentrations. MiSeq sequencing targeting 16S ribosomal DNA revealed that the airborne bacteria in desert area mainly belonged to the classes Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Bacilli, Alpha-proteobacteria, Beta-proteobacteria, and Gamma-proteobacteria. The bacterial community structures were different between dust events and non-dust events. The air samples collected at the dust events indicated high abundance rates of Alpha-proteobacteria, which were reported to dominate on the leaf surfaces of plants or in the saline lake environments. After the dust events, the members of Firmicutes (Bacilli) and Bacteroidetes, which are known to form endospore and attach with coarse particles, respectively, increased their relative abundances in the air samples. Presumably, the bacterial compositions and diversities in atmosphere significantly vary during dust events, which carry some particles from grassland (phyllo-sphere), dry lake, and sand surfaces, as well as some bacterial populations such as Firmicutes and Bacteroidetes maintain in the atmosphere for longer time.