Temporal dynamics of microbial transcription in wetted hyperarid desert soils.

Rainfall is rare in hyperarid deserts but, when it occurs, it triggers large biological responses essential for the long-term maintenance of the ecosystem. In drylands, microbes play major roles in nutrient cycling, but their responses to short-lived opportunity windows are poorly understood. Due to its ephemeral nature, mRNA is ideally suited to study microbiome dynamics upon abrupt changes in the environment. We analyzed microbial community transcriptomes after simulated rainfall in a Namib Desert soil over 7 days. Using total mRNA from dry and watered plots we infer short-term functional responses in the microbiome. A rapid two-phase cycle of activation and return to basal state was completed in a short period. Motility systems activated immediately, whereas competition-toxicity increased in parallel to predator taxa and the drying of soils. Carbon fixation systems were downregulated, and reactivated upon return to a near-dry state. The chaperone HSP20 was markedly regulated by watering across all major bacteria, suggesting a particularly important role in adaptation to desiccated ecosystems. We show that transcriptomes provide consistent and high resolution information on microbiome processes in a low-biomass environment, revealing shared patterns across taxa. We propose a structured dispersal-predation dynamic as a central driver of desert microbial responses to rainfall.

Documenting the diversity of the Namibian Ju|'hoansi intestinal microbiome.

We investigate the bacterial and fungal composition and functionality of the Ju|'hoansi intestinal microbiome (IM). The Juǀ'hoansi are a hunter-gatherer community residing in northeastern Namibia. They formerly subsisted by hunting and gathering but have been increasingly exposed to industrial dietary sources, medicines, and lifestyle features. They present an opportunity to study the evolution of the human IM in situ, from a predominantly hunter-gatherer to an increasingly Western urban-forager-farmer lifestyle. Their bacterial IM resembles that of typical hunter-gatherers, being enriched for genera such as Prevotella, Blautia, Faecalibacterium, Succinivibrio, and Treponema. Fungal IM inhabitants include animal pathogens and plant saprotrophs such as Fusarium, Issatchenkia, and Panellus. Our results suggest that diet and culture exert a greater influence on Ju|'hoansi IM composition than age, self-identified biological sex, and medical history. The Ju|'hoansi exhibit a unique core IM composition that diverges from the core IMs of other populations.

With a pinch of salt: metagenomic insights into Namib Desert salt pan microbial mats and halites reveal functionally adapted and competitive communities.

IMPORTANCE: The hyperarid Namib Desert is one of the oldest deserts on Earth. It contains multiple clusters of playas which are saline-rich springs surrounded by halite evaporites. Playas are of great ecological importance, and their indigenous (poly)extremophilic microorganisms are potentially involved in the precipitation of minerals such as carbonates and sulfates and have been of great biotechnological importance. While there has been a considerable amount of microbial ecology research performed on various Namib Desert edaphic microbiomes, little is known about the microbial communities inhabiting its multiple playas. In this work, we provide a comprehensive taxonomic and functional potential characterization of the microbial, including viral, communities of sediment mats and halites from two distant salt pans of the Namib Desert, contributing toward a better understanding of the ecology of this biome.

'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.

Rickettsia felis DNA recovered from a child who lived in southern Africa 2000 years ago.

The Stone Age record of South Africa provides some of the earliest evidence for the biological and cultural origins of Homo sapiens. While there is extensive genomic evidence for the selection of polymorphisms in response to pathogen-pressure in sub-Saharan Africa, e.g., the sickle cell trait which provides protection against malaria, there is inadequate direct human genomic evidence for ancient human-pathogen infection in the region. Here, we analysed shotgun metagenome libraries derived from the sequencing of a Later Stone Age hunter-gatherer child who lived near Ballito Bay, South Africa, c. 2000 years ago. This resulted in the identification of ancient DNA sequence reads homologous to Rickettsia felis, the causative agent of typhus-like flea-borne rickettsioses, and the reconstruction of an ancient R. felis genome.

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.

Diamonds in the rough: Dryland microorganisms are ecological engineers to restore degraded land and mitigate desertification.

Our planet teeters on the brink of massive ecosystem collapses, and arid regions experience manifold environmental and climatic challenges that increase the magnitude of selective pressures on already stressed ecosystems. Ultimately, this leads to their aridification and desertification, that is, to simplified and barren ecosystems (with proportionally less microbial load and diversity) with altered functions and food webs and modification of microbial community network. Thus, preserving and restoring soil health in such a fragile biome could help buffer climate change's effects. We argue that microorganisms and the protection of their functional properties and networks are key to fight desertification. Specifically, we claim that it is rational, possible and certainly practical to rely on native dryland edaphic microorganisms and microbial communities as well as dryland plants and their associated microbiota to conserve and restore soil health and mitigate soil depletion in newly aridified lands. Furthermore, this will meet the objective of protecting/stabilizing (and even enhancing) soil biodiversity globally. Without urgent conservation and restoration actions that take into account microbial diversity, we will ultimately, and simply, not have anything to protect anymore.

Microbial Biogeochemical Cycling of Nitrogen in Arid Ecosystems.

Arid ecosystems cover ∼40% of the Earth's terrestrial surface and store a high proportion of the global nitrogen (N) pool. They are low-productivity, low-biomass, and polyextreme ecosystems, i.e., with (hyper)arid and (hyper)oligotrophic conditions and high surface UV irradiation and evapotranspiration. These polyextreme conditions severely limit the presence of macrofauna and -flora and, particularly, the growth and productivity of plant species. Therefore, it is generally recognized that much of the primary production (including N-input processes) and nutrient biogeochemical cycling (particularly N cycling) in these ecosystems are microbially mediated. Consequently, we present a comprehensive survey of the current state of knowledge of biotic and abiotic N-cycling processes of edaphic (i.e., open soil, biological soil crust, or plant-associated rhizosphere and rhizosheath) and hypo/endolithic refuge niches from drylands in general, including hot, cold, and polar desert ecosystems. We particularly focused on the microbially mediated biological nitrogen fixation, N mineralization, assimilatory and dissimilatory nitrate reduction, and nitrification N-input processes and the denitrification and anaerobic ammonium oxidation (anammox) N-loss processes. We note that the application of modern meta-omics and related methods has generated comprehensive data sets on the abundance, diversity, and ecology of the different N-cycling microbial guilds. However, it is worth mentioning that microbial N-cycling data from important deserts (e.g., Sahara) and quantitative rate data on N transformation processes from various desert niches are lacking or sparse. Filling this knowledge gap is particularly important, as climate change models often lack data on microbial activity and environmental microbial N-cycling communities can be key actors of climate change by producing or consuming nitrous oxide (N2O), a potent greenhouse gas.

The plant rhizosheath-root niche is an edaphic "mini-oasis" in hyperarid deserts with enhanced microbial competition.

Plants have evolved unique morphological and developmental adaptations to cope with the abiotic stresses imposed by (hyper)arid environments. Such adaptations include the formation of rhizosheath-root system in which mutualistic plant-soil microbiome associations are established: the plant provides a nutrient-rich and shielded environment to microorganisms, which in return improve plant-fitness through plant growth promoting services. We hypothesized that the rhizosheath-root systems represent refuge niches and resource islands for the desert edaphic microbial communities. As a corollary, we posited that microorganisms compete intensively to colonize such "oasis" and only those beneficial microorganisms improving host fitness are preferentially selected by plant. Our results show that the belowground rhizosheath-root micro-environment is largely more hospitable than the surrounding gravel plain soil with higher nutrient and humidity contents, and cooler temperatures. By combining metabarcoding and shotgun metagenomics, we demonstrated that edaphic microbial biomass and community stability increased from the non-vegetated soils to the rhizosheath-root system. Concomitantly, non-vegetated soil communities favored autotrophy lifestyle while those associated with the plant niches were mainly heterotrophs and enriched in microbial plant growth promoting capacities. An intense inter-taxon microbial competition is involved in the colonization and homeostasis of the rhizosheath zone, as documented by significant enrichment of antibiotic resistance genes and CRISPR-Cas motifs. Altogether, our results demonstrate that rhizosheath-root systems are "edaphic mini-oases" and microbial diversity hotspots in hyperarid deserts. However, to colonize such refuge niches, the desert soil microorganisms compete intensively and are therefore prepared to outcompete potential rivals.

Multi-proxy analyses of a mid-15th century Middle Iron Age Bantu-speaker palaeo-faecal specimen elucidates the configuration of the 'ancestral' sub-Saharan African intestinal microbiome.

BACKGROUND: The archaeological incidence of ancient human faecal material provides a rare opportunity to explore the taxonomic composition and metabolic capacity of the ancestral human intestinal microbiome (IM). Here, we report the results of the shotgun metagenomic analyses of an ancient South African palaeo-faecal specimen. METHODS: Following the recovery of a single desiccated palaeo-faecal specimen from Bushman Rock Shelter in Limpopo Province, South Africa, we applied a multi-proxy analytical protocol to the sample. The extraction of ancient DNA from the specimen and its subsequent shotgun metagenomic sequencing facilitated the taxonomic and metabolic characterisation of this ancient human IM. RESULTS: Our results indicate that the distal IM of the Neolithic 'Middle Iron Age' (c. AD 1460) Bantu-speaking individual exhibits features indicative of a largely mixed forager-agro-pastoralist diet. Subsequent comparison with the IMs of the Tyrolean Iceman (Ötzi) and contemporary Hadza hunter-gatherers, Malawian agro-pastoralists and Italians reveals that this IM precedes recent adaptation to 'Western' diets, including the consumption of coffee, tea, chocolate, citrus and soy, and the use of antibiotics, analgesics and also exposure to various toxic environmental pollutants. CONCLUSIONS: Our analyses reveal some of the causes and means by which current human IMs are likely to have responded to recent dietary changes, prescription medications and environmental pollutants, providing rare insight into human IM evolution following the advent of the Neolithic c. 12,000 years ago. Video Abtract.

Nutrient Acquisition, Rather Than Stress Response Over Diel Cycles, Drives Microbial Transcription in a Hyper-Arid Namib Desert Soil.

Hot desert surface soils are characterized by extremely low water activities for large parts of any annual cycle. It is widely assumed that microbial processes in such soils are very limited. Here we present the first metatranscriptomic survey of microbial community function in a low water activity hyperarid desert soil. Sequencing of total mRNA revealed a diverse and active community, dominated by Actinobacteria. Metatranscriptomic analysis of samples taken at different times over 3 days indicated that functional diel variations were limited at the whole community level, and mostly affected the eukaryotic subpopulation which was induced during the cooler night hours. High levels of transcription of chemoautotrophic carbon fixation genes contrasted with limited expression of photosynthetic genes, indicating that chemoautotrophy is an important alternative to photosynthesis for carbon cycling in desiccated desert soils. Analysis of the transcriptional levels of key N-cycling genes provided strong evidence that soil nitrate was the dominant nitrogen input source. Transcriptional network analyses and taxon-resolved functional profiling suggested that nutrient acquisition processes, and not diurnal environmental variation, were the main drivers of community activity in hyperarid Namib Desert soil. While we also observed significant levels of expression of common stress response genes, these genes were not dominant hubs in the co-occurrence network.

Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host.

BACKGROUND: The rhizosheath-root system is an adaptive trait of sandy-desert speargrasses in response to unfavourable moisture and nutritional conditions. Under the deserts' polyextreme conditions, plants interact with edaphic microorganisms that positively affect their fitness and resistance. However, the trophic simplicity and environmental harshness of desert ecosystems have previously been shown to strongly influence soil microbial community assembly. We hypothesize that sand-driven ecological filtering constrains the microbial recruitment processes in the speargrass rhizosheath-root niche, prevailing over the plant-induced selection. METHODS: Bacterial and fungal communities from the rhizosheath-root compartments (endosphere root tissues, rhizosheath and rhizosphere) of three Namib Desert speargrass species (Stipagrostis sabulicola, S. seelyae and Cladoraphis spinosa) along with bulk sand have been studied to test our hypothesis. To minimize the variability determined by edaphic and climatic factors, plants living in a single dune were studied. We assessed the role of plant species vs the sandy substrate on the recruitment and selection, phylogenetic diversity and co-occurrence microbial networks of the rhizosheath-root system microbial communities. RESULTS: Microorganisms associated with the speargrass rhizosheath-root system were recruited from the surrounding bulk sand population and were significantly enriched in the rhizosheath compartments (105 and 104 of bacterial 16S rRNA and fungal ITS copies per gram of sand to up to 108 and 107 copies per gram, respectively). Furthermore, each rhizosheath-root system compartment hosted a specific microbial community demonstrating strong niche-partitioning. The rhizosheath-root systems of the three speargrass species studied were dominated by desert-adapted Actinobacteria and Alphaproteobacteria (e.g. Lechevalieria, Streptomyces and Microvirga) as well as saprophytic Ascomycota fungi (e.g. Curvularia, Aspergillus and Thielavia). Our results clearly showed a random phylogenetic turnover of rhizosheath-root system associated microbial communities, independent of the plant species, where stochastic factors drive neutral assembly. Co-occurrence network analyses also indicated that the bacterial and fungal community members of the rhizosheath-root systems established a higher number of interactions than those in the barren bulk sand, suggesting that the former are more stable and functional than the latter. CONCLUSION: Our study demonstrates that the rhizosheath-root system microbial communities of desert dune speargrasses are stochastically assembled and host-independent. This finding supports the concept that the selection determined by the desert sand prevails over that imposed by the genotype of the different plant species.

Namib Desert primary productivity is driven by cryptic microbial community N-fixation.

Carbon exchange in drylands is typically low, but during significant rainfall events (wet anomalies) drylands act as a C sink. During these anomalies the limitation on C uptake switches from water to nitrogen. In the Namib Desert of southern Africa, the N inventory in soil organic matter available for mineralisation is insufficient to support the observed increase in primary productivity. The C4 grasses that flourish after rainfall events are not capable of N fixation, and so there is no clear mechanism for adequate N fixation in dryland ecosystems to support rapid C uptake. Here we demonstrate that N fixation by photoautotrophic hypolithic communities forms the basis for the N budget for plant productivity events in the Namib Desert. Stable N isotope (δ15N) values of Namib Desert hypolithic biomass, and surface and subsurface soils were measured over 3 years across dune and gravel plain biotopes. Hypoliths showed significantly higher biomass and lower δ15N values than soil organic matter. The δ15N values of hypoliths approach the theoretical values for nitrogen fixation. Our results are strongly indicative that hypolithic communities are the foundation of productivity after rain events in the Namib Desert and are likely to play similar roles in other arid environments.

Namib Desert Soil Microbial Community Diversity, Assembly, and Function Along a Natural Xeric Gradient.

The hyperarid Namib desert is a coastal desert in southwestern Africa and one of the oldest and driest deserts on the planet. It is characterized by a west/east increasing precipitation gradient and by regular coastal fog events (extending up to 75 km inland) that can also provide soil moisture. In this study, we evaluated the role of this natural aridity and xeric gradient on edaphic microbial community structure and function in the Namib desert. A total of 80 individual soil samples were collected at 10-km intervals along a 190-km transect from the fog-dominated western coastal region to the eastern desert boundary. Seventeen physicochemical parameters were measured for each soil sample. Soil parameters reflected the three a priori defined climatic/xeric zones along the transect ("fog," "low rain," and "high rain"). Microbial community structures were characterized by terminal restriction fragment length polymorphism fingerprinting and shotgun metaviromics, and their functional capacities were determined by extracellular enzyme activity assays. Both microbial community structures and activities differed significantly between the three xeric zones. The deep sequencing of surface soil metavirome libraries also showed shifts in viral composition along the xeric transect. While bacterial community assembly was influenced by soil chemistry and stochasticity along the transect, variations in community "function" were apparently tuned by xeric stress.

Bacterial nitrogen fixation in sand bioreactors treating winery wastewater with a high carbon to nitrogen ratio.

Heterotrophic bacteria proliferate in organic-rich environments and systems containing sufficient essential nutrients. Nitrogen, phosphorus and potassium are the nutrients required in the highest concentrations. The ratio of carbon to nitrogen is an important consideration for wastewater bioremediation because insufficient nitrogen may result in decreased treatment efficiency. It has been shown that during the treatment of effluent from the pulp and paper industry, bacterial nitrogen fixation can supplement the nitrogen requirements of suspended growth systems. This study was conducted using physicochemical analyses and culture-dependent and -independent techniques to ascertain whether nitrogen-fixing bacteria were selected in biological sand filters used to treat synthetic winery wastewater with a high carbon to nitrogen ratio (193:1). The systems performed well, with the influent COD of 1351 mg/L being reduced by 84-89%. It was shown that the nitrogen fixing bacterial population was influenced by the presence of synthetic winery effluent in the surface layers of the biological sand filters, but not in the deeper layers. It was hypothesised that this was due to the greater availability of atmospheric nitrogen at the surface. The numbers of culture-able nitrogen-fixing bacteria, including presumptive Azotobacter spp. exhibited 1-2 log increases at the surface. The results of this study confirm that nitrogen fixation is an important mechanism to be considered during treatment of high carbon to nitrogen wastewater. If biological treatment systems can be operated to stimulate this phenomenon, it may obviate the need for nitrogen addition.

Ancient oncogenesis, infection and human evolution.

The recent discovery that malignant neoplastic lesions date back nearly 2 million years ago not only highlights the antiquity of cancer in the human lineage, but also provides remarkable insight into ancestral hominin disease pathology. Using these Early Pleistocene examples as a point of departure, we emphasize the prominent role of viral and bacterial pathogens in oncogenesis and evaluate the impact of pathogens on human evolutionary processes in Africa. In the Shakespearean vernacular "what's past is prologue," we highlight the significance of novel information derived from ancient pathogenic DNA. In particular, and given the temporal depth of human occupation in sub-Saharan Africa, it is emphasized that the region is ideally positioned to play a strategic role in the discovery of ancient pathogenic drivers of not only human mortality, but also human evolution. Ancient African pathogen genome data can provide novel revelations concerning human-pathogen coevolutionary processes, and such knowledge is essential for forecasting the ways in which emerging zoonotic and increasingly transmissible diseases might influence human demography and longevity in the future.

Assembling metagenomes, one community at a time.

BACKGROUND: Metagenomics allows unprecedented access to uncultured environmental microorganisms. The analysis of metagenomic sequences facilitates gene prediction and annotation, and enables the assembly of draft genomes, including uncultured members of a community. However, while several platforms have been developed for this critical step, there is currently no clear framework for the assembly of metagenomic sequence data. RESULTS: To assist with selection of an appropriate metagenome assembler we evaluated the capabilities of nine prominent assembly tools on nine publicly-available environmental metagenomes, as well as three simulated datasets. Overall, we found that SPAdes provided the largest contigs and highest N50 values across 6 of the 9 environmental datasets, followed by MEGAHIT and metaSPAdes. MEGAHIT emerged as a computationally inexpensive alternative to SPAdes, assembling the most complex dataset using less than 500 GB of RAM and within 10 hours. CONCLUSIONS: We found that assembler choice ultimately depends on the scientific question, the available resources and the bioinformatic competence of the researcher. We provide a concise workflow for the selection of the best assembly tool.

Migrating microbes: what pathogens can tell us about population movements and human evolution.

BACKGROUND: The biology of human migration can be observed from the co-evolutionary relationship with infectious diseases. While many pathogens are brief, unpleasant visitors to human bodies, others have the ability to become life-long human passengers. The story of a pathogen's genetic code may, therefore, provide insight into the history of its human host. The evolution and distribution of disease in Africa is of particular interest, because of the deep history of human evolution in Africa, the presence of a variety of non-human primates, and tropical reservoirs of emerging infectious diseases. METHODS: This study explores which pathogens leave traces in the archaeological record, and whether there are realistic prospects that these pathogens can be recovered from sub-Saharan African archaeological contexts. RESULTS: Three stories are then presented of germs on a journey. The first is the story of HIV's spread on the back of colonialism and the railway networks over the last 150 years. The second involves the spread of Schistosoma mansoni, a parasite which shares its history with the trans-Atlantic slave trade and the origins of fresh-water fishing. Finally, we discuss the tantalising hints of hominin migration and interaction found in the genome of human herpes simplex virus 2. CONCLUSIONS: Evidence from modern African pathogen genomes can provide data on human behaviour and migration in deep time and contribute to the improvement of human quality-of-life and longevity.

Metaviromes of Extracellular Soil Viruses along a Namib Desert Aridity Gradient.

The Namib Desert in southwest Africa is hyperarid and composed of distinct microbial communities affected by a longitudinal aridity gradient. Here, we report four soil metaviromes from the Namib Desert, assessed using deep sequencing of metavirome libraries prepared from DNA extracted from gravel plain surface soils.

Namib Desert edaphic bacterial, fungal and archaeal communities assemble through deterministic processes but are influenced by different abiotic parameters.

The central Namib Desert is hyperarid, where limited plant growth ensures that biogeochemical processes are largely driven by microbial populations. Recent research has shown that niche partitioning is critically involved in the assembly of Namib Desert edaphic communities. However, these studies have mainly focussed on the Domain Bacteria. Using microbial community fingerprinting, we compared the assembly of the bacterial, fungal and archaeal populations of microbial communities across nine soil niches from four Namib Desert soil habitats (riverbed, dune, gravel plain and salt pan). Permutational multivariate analysis of variance indicated that the nine soil niches presented significantly different physicochemistries (R 2 = 0.8306, P ≤ 0.0001) and that bacterial, fungal and archaeal populations were soil niche specific (R 2 ≥ 0.64, P ≤ 0.001). However, the abiotic drivers of community structure were Domain-specific (P < 0.05), with P, clay and sand fraction, and NH4 influencing bacterial, fungal and archaeal communities, respectively. Soil physicochemistry and soil niche explained over 50% of the variation in community structure, and communities displayed strong non-random patterns of co-occurrence. Taken together, these results demonstrate that in central Namib Desert soil microbial communities, assembly is principally driven by deterministic processes.