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Cowan, D. A.

Publications and source records attributed to Cowan, D. A..

14 recordsLinked to original sources

Trace gas oxidation supports sub-surface microbial communities across Namib Desert fog and aridity gradients

Widely accepted climate predictions indicate that drylands will expand to cover more than half of the Earths terrestrial surface by the end of the 21st century. In these environments, harsh conditions including nutrient and water limitations restrict plant and animal life, thereby increasing the importance of soil microbial communities in nutrient cycling and ecosystem functioning. The Namib Desert is a distinctive dryland ecosystem characterised by a steep natural aridity gradient, transitioning from a coastal hyperarid zone influenced by frequent fog deposition to an inland arid region receiving seasonal rainfall. This study investigates the impact of water availability and moisture regime on microbial trace gas oxidation and community composition across this aridity gradient. Quantitative analyses revealed that total microbial abundance and activity indicators, including ATP concentrations and respiration rates, were significantly (p < 0.005) reduced in hyperarid soils compared to their arid counterparts. In contrast, hyperarid fog-dominated soils exhibited significantly (p < 0.0005) elevated rates of atmospheric hydrogen oxidation, even in the absence of water inputs. We propose that sustained high-affinity hydrogen oxidation, coupled with rapid microbial resuscitation following wetting events, supports shallow sub-surface microbial communities in the Namib Desert, particularly in the coastal hyperarid zone. Together, these findings challenge current understanding of the lower limits of microbial activity and reveal alternate metabolic pathways that enable microbial persistence in hyperarid hot desert soils. ImportanceDrylands are expanding globally, yet the mechanisms that allow microbial life to persist under extreme and sustained water limitation remain poorly understood. This study demonstrates that atmospheric trace gas oxidation, particularly high-affinity hydrogen oxidation, supports active and resilient microbial communities in hyperarid soils of the Namib Desert, even in the absence of liquid water inputs. By revealing how microbes may couple trace gas metabolism to energy and water generation, our findings provide new insight into the lower limits of microbial activity in dry hot desert soils and highlight the need to investigate how microbes persist and sustain soil ecosystem functioning.

microbiology↗

Aridity drives global convergence of desert microbiomes and biogeochemical activities

Deserts cover a third of the worlds surface, supporting unique biomes and ecosystem services. Yet, we lack a comprehensive assessment of what defines and drives the microbial communities that dominate life in these regions. Here, we conducted a standardized field survey in contrasting cold, hot, and polar deserts across the seven continents, and observed geographically distant deserts share similar structure, function, and activities. Desert communities are dominated by genomically streamlined Actinobacteriota and Chloroflexota, and compared with non-desert soils, are significantly enriched with stress tolerance genes, mobile genetic elements, and antiviral strategies, revealing previously unknown ecological and evolutionary dynamics. Metabolically, these communities exhibit reduced capacity for carbohydrate and protein degradation, and instead are enriched for chemosynthetic carbon fixation, continuous energy harvesting using atmospheric trace gases and sunlight, and energy reserve biosynthesis. All sampled soils mediated respiration, trace gas oxidation, and carbon fixation, with detectable activity even in hyper-arid Atacama and Antarctic soils at the margins of life. Driver analyses identified aridity as the primary overriding driver of the microbial communities and biogeochemical activities. Collectively, these findings suggest that aridity selects for metabolically self-sufficient taxa capable of continuously meeting energy and carbon needs independently of vegetation-derived inputs, while enduring physicochemical stressors and potentially elevated viral pressure. These new insights are integral to forecast the future of soils amid increasing desertification. Significance statementDesert soils occupy a vast and expanding portion of Earth, yet what defines and governs their dominant microbial life remains incompletely defined. By assessing the composition, capabilities, and activities of microbial communities across deserts on all seven continents, we identify unifying signatures of life under extreme water limitation. We show microbial communities are highly self-sufficient, capable of acquiring energy and carbon even where plant inputs are minimal. This planetary-scale understanding of the desert microbiome has important ramifications for forecasting potential shifts of microbial communities and the services they provide as desertification intensifies.

microbiology↗

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

Salt pans or playas, which are saline-rich springs surrounded by halite evaporates in arid environments, have played an essential role in landscape erosion during the formation of the Namib Desert and are numerous in its central region. In this study, we used shotgun metagenomics to investigate the phylogenetic and functional capacities of the microbial communities from two salt pans (namely, Eisefeld and Hosabes) located in the Central Namib Desert, located in Southwest Africa. We studied the source and sink sediment mat communities of the saline streams, as well as those from two halites (crystallized structures on the stream margins). The microbial assemblages and potential functions were distinct in both niches. Independently from their localization (Eisfeld vs Hosabes and source vs sink), the sediment mat communities were dominated by members of the Alpha- and Gamma-proteobacteria classes, while halites were Archaea-dominated and also contained high abundances of the extremely halophilic bacterium Salinibacter sp. (phylum Bacteroidota). Photoheterotrophy and chemoheterotrophy were the principal lifestyles in both niches, with halite communities having a reduced diversity of metabolic pathways. Intense microbial-virus interactions in both niches were implied by the widespread detection of CRISPR-Cas defense systems. We identified a putatively novel clade of type II CRISPR-Cas systems, as well as novel candidate viral lineages of the class Caudoviricetes and of Halobacteriales-infecting haloviruses. Putative gene transfer agent-like sequences within the Alphaproteobacteria were identified in the sediment mat communities. These horizontal gene transfer elements have the potential to drive genome plasticity and evolution of the Alphaproteobacteria in the Namib Desert salt pan microbiomes. ImportanceThe 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 preformed on various Namib Desert edaphic microbiomes, little is known about the microbial communities inhabiting its multiple playas. In this work, we therefore provide a comprehensive taxonomic and functional potential characterization of the microbial, including viral, communities of sediment mats and halites from two distant Namib Desert, contributing towards a better understanding of the ecology of this biome.

microbiology↗

TREM2+ and interstitial macrophages orchestrate airway inflammation in SARS-CoV-2 infection in rhesus macaques

The COVID-19 pandemic remains a global health crisis, yet, the immunopathological mechanisms driving the development of severe disease remain poorly defined. Here, we utilize a rhesus macaque (RM) model of SARS-CoV-2 infection to delineate perturbations in the innate immune system during acute infection using an integrated systems analysis. We found that SARS-CoV-2 initiated a rapid infiltration (two days post infection) of plasmacytoid dendritic cells into the lower airway, commensurate with IFNA production, natural killer cell activation, and induction of interferon-stimulated genes. At this early interval, we also observed a significant increase of blood CD14-CD16+ monocytes. To dissect the contribution of lung myeloid subsets to airway inflammation, we generated a novel compendium of RM-specific lung macrophage gene expression using a combination of sc-RNA-Seq data and bulk RNA-Seq of purified populations under steady state conditions. Using these tools, we generated a longitudinal sc-RNA-seq dataset of airway cells in SARS-CoV-2-infected RMs. We identified that SARS-CoV-2 infection elicited a rapid recruitment of two subsets of macrophages into the airway: a C206+MRC1-population resembling murine interstitial macrophages, and a TREM2+ population consistent with CCR2+ infiltrating monocytes, into the alveolar space. These subsets were the predominant source of inflammatory cytokines, accounting for ~75% of IL6 and TNF production, and >90% of IL10 production, whereas the contribution of CD206+MRC+ alveolar macrophages was significantly lower. Treatment of SARS-CoV-2 infected RMs with baricitinib (Olumiant(R)), a novel JAK1/2 inhibitor that recently received Emergency Use Authorization for the treatment of hospitalized COVID-19 patients, was remarkably effective in eliminating the influx of infiltrating, non-alveolar macrophages in the alveolar space, with a concomitant reduction of inflammatory cytokines. This study has delineated the major subsets of lung macrophages driving inflammatory and anti-inflammatory cytokine production within the alveolar space during SARS-CoV-2 infection. One sentence summaryMulti-omic analyses of hyperacute SARS-CoV-2 infection in rhesus macaques identified two population of infiltrating macrophages, as the primary orchestrators of inflammation in the lower airway that can be successfully treated with baricitinib

microbiology↗

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 which are considered to be essential for the long-term maintenance of biodiversity. In such environments, microbial communities have major roles in nutrient cycling, but their functional responses to short-lived resource opportunities are poorly understood. We used whole community metatranscriptomic data to demonstrate structured and sequential functional responses in desiccated desert soils to a simulated rainfall event over a seven-day time frame. Rapid transcriptional activation of Actinobacteria, Alpha-proteobacteria and phage transcripts was followed by a marked increase in protist and myxobacterial activity, before returning to the original state. In functional terms, motility systems were activated in the early phases, whereas competition-toxicity systems increased in parallel to the activity from predators and the drying of soils. The dispersal-predation dynamic was identified as a central driver of microbial community responses to watering. Carbon fixation mechanisms that were active under dry condition were rapidly down-regulated in wetted soils, and only reactivated on a return to a near-dry state, suggesting a reciprocal balance between carbon fixation and fixed-carbon acquisition processes. Water addition induced a general reduction in the transcription of stress response genes, most prominently HSP20, indicating that this chaperone is particularly important for life in desiccated ecosystems. Based on these data, we propose a rainfall response model for desert soil microbiomes.

microbiology↗

CCR2-dependent monocyte-derived cells restrict SARS-CoV-2 infection

SARS-CoV-2 has caused a historic pandemic of respiratory disease (COVID-19) and current evidence suggests severe disease is associated with dysregulated immunity within the respiratory tract. However, the innate immune mechanisms that mediate protection during COVID-19 are not well defined. Here we characterize a mouse model of SARS-CoV-2 infection and find that early CCR2-dependent infiltration of monocytes restricts viral burden in the lung. We find that a recently developed mouse-adapted MA-SARS-CoV-2 strain, as well as the emerging B. 1.351 variant, trigger an inflammatory response in the lung characterized by expression of pro-inflammatory cytokines and interferon-stimulated genes. scRNA-seq analysis of lung homogenates identified a hyper-inflammatory monocyte profile. Using intravital antibody labeling, we demonstrate that MA-SARS-CoV-2 infection leads to increases in circulating monocytes and an influx of CD45+ cells into the lung parenchyma that is dominated by monocyte-derived cells. We utilize this model to demonstrate that mechanistically, CCR2 signaling promotes infiltration of classical monocytes into the lung and expansion of monocyte-derived cells. Parenchymal monocyte-derived cells appear to play a protective role against MA-SARS-CoV-2, as mice lacking CCR2 showed higher viral loads in the lungs, increased lung viral dissemination, and elevated inflammatory cytokine responses. These studies have identified a CCR2-monocyte axis that is critical for promoting viral control and restricting inflammation within the respiratory tract during SARS-CoV-2 infection.

immunology↗

A genome compendium reveals diverse metabolic adaptations of Antarctic soil microorganisms

A surprising diversity and abundance of microorganisms resides in the cold desert soils of Antarctica. The metabolic processes that sustain them, however, are poorly understood. In this study, we used metagenomic and biogeochemical approaches to study the microbial communities in 16 physicochemically diverse mountainous and glacial soils from remote sites in South Victoria Land, north of the Mackay Glacier. We assembled 451 metagenome-assembled genomes from 18 bacterial and archaeal phyla, constituting the largest resource of Antarctic soil microbial genomes to date. The most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen and carbon monoxide to meet energy, carbon, and, through metabolic water production, hydration needs. Phylogenetic analysis and structural modelling infer that bacteria from nine phyla can scavenge atmospheric hydrogen using a previously unreported enzyme family, the group 1l [NiFe]-hydrogenases. Consistently, gas chromatography measurements confirmed most soils rapidly consume atmospheric hydrogen and carbon monoxide, and provide the first experimental evidence of methane oxidation in non-maritime Antarctica. We also recovered genomes of microorganisms capable of oxidizing other inorganic compounds, including nitrogen, sulfur, and iron compounds, as well as harvesting solar energy via photosystems and novel microbial rhodopsins. Bacterial lineages defined by symbiotic lifestyles, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also surprisingly abundant. We conclude that the dominant microorganisms in Antarctic soils adopt mixotrophic strategies for energy and sometimes carbon acquisition, though they co-exist with diverse bacteria and archaea that adopt more specialist lifestyles. These unprecedented insights and associated genome compendium will inform efforts to protect biodiversity in this continent.

microbiology↗

Ancient DNA of Rickettsia felis and Toxoplasma gondii implicated in the death of a hunter-gatherer boy from South Africa, 2,000 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, there is insufficient evidence for ancient human-pathogen interactions 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. 2,000 years ago. This resulted in the identification of DNA sequence reads homologous to Rickettsia felis, and the reconstruction of an ancient R. felis genome, the causative agent of typhus-like flea-borne rickettsioses. The concurrent detection of DNA reads derived from Toxoplasma gondii, the causative agent of toxoplasmosis, confirms the pre-Neolithic incidence of these pathogens in southern Africa. We demonstrate that an R. felis and T. gondii co-infection, exacerbated by various additional bacterial and parasitic pathogens, contributed to the ill-health and subsequent demise of the boy from Ballito Bay.

molecular biology↗

Nutrient parsimony shapes diversity and functionality in hyper-oligotrophic Antarctic soils

The balance of nutrients in soil is critical for microbial growth and function, and stoichiometric values below the Redfield ratio for C:N:P can negatively affect microbial ecosystem services. However, few studies have assessed the relationships between nutrient balance and biological productivity in extremely nutrient-poor habitats. The Mackay Glacier region of Eastern Antarctica is a hyper-oligotrophic ice-free desert and is an appropriate landscape to evaluate the effects of nutrient deficiency and imbalance on microbial community ecology. In a survey of multiple, widely dispersed soil samples from this region, we detected only low rates of microbial respiration, and observed that C:N:P ratios were well below those required for optimal activity. In silico metagenomic and soil isotopic ratio ({delta}15N) analyses indicated that the capacity for nitrogen fixation was low, but that soil microbial communities were enriched for soil nitrate assimilation processes, mostly associated with heterotrophic taxa.{delta} 13C isotope ratio data suggested that carbon dioxide was fixed principally via the Calvin cycle. Genes involved in this pathway were common to all metagenomes and were primarily attributed to members of the dominant soil bacterial phyla: Bacteroidetes and Acidobacteria. The identification of multiple genes encoding non-photoautotrophic RUBISCO and carbon dioxide dehydrogenase enzymes in both the metagenomic sequences and assembled MAGs is suggestive of a trace-gas scavenging physiology in members of these soil communities.

ecology↗

Phages actively challenge niche communities in the Antarctic soils

By modulating the structure, diversity and trophic outputs of microbial communities, phages play crucial roles in many biomes. In oligotrophic polar deserts, the effects of katabatic winds, constrained nutrients and low water availability are known to limit microbial activity. Although phages may substantially govern trophic interactions in cold deserts, relatively little is known regarding the precise ecological mechanisms. Here, we provide the first evidence of widespread antiphage innate immunity in Antarctic environments using metagenomic sequence data from hypolith communities as model systems. In particular, immunity systems such as DISARM and BREX are shown to be dominant systems in these communities. Additionally, we show a direct correlation between the CRISPR-cas adaptive immunity and the metavirome of hypolith communities, suggesting the existence of dynamic hostphage interactions. In addition to providing the first exploration of immune systems in cold deserts, our results suggest that phages actively challenge niche communities in Antarctic polar deserts. We provide evidence suggesting that the regulatory role played by phages in this system is an important determinant of bacterial host interactions in this environment. ImportanceIn Antarctic environments, the combination of both abiotic and biotic stressors results in simple trophic levels dominated by microbiomes. Although the past two decades have revealed substantial insights regarding the diversity and structure of microbiomes, we lack mechanistic insights regarding community interactions and how phages may affect these. By providing the first evidence of widespread antiphage innate immunity, we shed light on phage-host dynamics in Antarctic niche communities. Our analyses reveal several antiphage defense systems including DISARM and BREX, which appear to dominate in cold desert niche communities. In contrast, our analyses revealed that genes, which encode antiphage adaptive immunity were under-represented in these communities suggesting lower infection frequencies in cold edaphic environments. We propose that by actively challenging niche communities, phages play crucial roles in the diversification of Antarctic communities.

microbiology↗

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

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). 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. Our results indicate that the distal IM of the Neolithic Middle Iron Age (c. AD 1485) Bantu-speaking individual exhibits features indicative of a largely mixed forager-agro-pastoralist diet. Subsequent comparison with the IMs of the Tyrolean Iceman (Otzi) 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. 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.

microbiology↗

Trophic Selective Pressures Organize the Composition of Endolithic Microbial Communities from Global Deserts

Studies of microbial biogeography are often convoluted by extremely high diversity and differences in microenvironmental factors such as pH and nutrient availability. Desert endolithic (inside rock) communities are exceptionally simple ecosystems that can serve as a tractable model for investigating long-range biogeographic effects on microbial communities. We conducted a comprehensive survey of endolithic sandstones using high-throughput marker gene sequencing to characterize global patterns of diversity in endolithic microbial communities. We also tested a range of abiotic variables in order to investigate the factors that drive community assembly at various trophic levels. Macroclimate was found to be the primary driver of endolithic community composition, with the most striking difference witnessed between hot and polar deserts. This difference was largely attributable to the specialization of prokaryotic and eukaryotic primary producers to different climate conditions. On a regional scale, microclimate and properties of the rock substrate were found to influence community assembly, although to a lesser degree than global hot versus polar conditions. We found new evidence that the factors driving endolithic community assembly differ between trophic levels. While phototrophic taxa were rigorously selected for among different sites, heterotrophic taxa were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph assembly. This study is the first to uncover the global drivers of desert endolithic diversity using high-throughput sequencing. We demonstrate that phototrophs and heterotrophs in the endolithic community assemble under different stochastic and deterministic influences, emphasizing the need for studies of microorganisms in context of their functional niche in the community.

microbiology↗

Nutrient acquisition, rather than stress response over diel cycles, drives microbial transcription in a dessicated Namib Desert soil

Hot desert surface soils are characterised 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 three days indicated that most functions did not fluctuate on a diel basis, except for a 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.

ecology↗

Assembling Metagenomes, One Community At A Time

Metagenomics allows unprecedented access to uncultured environmental microorganisms. The assembly of metagenomic sequences facilitates gene prediction and annotation, and enables the assembly of draft genomes of dominant taxa, including uncultured members of a community. However, while numerous platforms have been developed for this critical step, there is currently no strict standard for the assembly of metagenomic sequence data. To assist with selection of an appropriate metagenome assembler we evaluated the capabilities of eight prominent assembly tools on nine publicly-available environmental metagenomes. We found that assembler choice ultimately hinges on the scientific question at hand, the resources available and the bioinformatic competence of the researcher. We provide a concise workflow for the selection of the best assembly tool.

bioinformatics↗