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Chown, S. L.

Publications and source records attributed to Chown, S. L..

15 recordsLinked to original sources

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↗

Widespread horizontal transfer and strong selection enhance microbial adaptation in Antarctic soils

Terrestrial Antarctica harbors compositionally diverse and functionally distinct microbial life. Yet the ecological and evolutionary processes enabling these communities to adapt to the polyextreme conditions of the continent remain largely unknown. Here, we address how horizontal gene transfer (HGT) and de novo mutations influence adaptation of microbial communities in 16 proglacial and mountainous Antarctic soils, from a combination of short- and long-read datasets. Phylogenetic reconciliation and mobile genetic element analysis of 676 metagenome-assembled genomes show that HGT events occur frequently within these microbial communities. While the transferred genes are distributed across diverse functional categories, those involved in energy metabolism are exchanged at relatively higher frequency. The genes for aerotrophy, i.e. the consumption of atmospheric trace gases to provide energy, carbon, and hydration, are among the most frequently and widely disseminated. Approximately a quarter of all carbon monoxide (CO) dehydrogenases and [NiFe]-hydrogenases that catalyze atmospheric CO and hydrogen (H2) oxidation are predicted to be horizontally acquired and are often closely associated with mobile genetic elements. In parallel, analysis of polymorphisms in protein-encoding genes suggests widespread purifying selection, demonstrated by a predominance of synonymous mutations. This selection is particularly intense for aerotrophy genes, providing further evidence that this process is critical for microbial survival in Antarctica. The genetic variation of hydrogenases is tightly associated with their predicted protein structures, with intense selection acting on critical sites that preserve their stability and function in Antarctic environments. Together, these findings show that previously unrecognised eco-evolutionary dynamics shape the composition and function of Antarctic desert microbial communities, and confirm aerotrophy is a strongly selected and horizontally disseminated trait.

microbiology↗

Resilient Antarctic soil bacteria consume trace gases across wide temperature ranges

Polar desert soils host diverse microbial communities despite limited nutrients and frequent temperature and light fluctuations. Adapting to these extremes, most bacteria possess high-affinity hydrogenases and carbon monoxide dehydrogenases, enabling them to use atmospheric trace gases such as hydrogen (H2) and carbon monoxide (CO) to generate energy and fix carbon. Despite the foundational importance of this process in polar desert ecosystems, little is known about the thermal sensitivity of trace gas oxidation or how this process will respond to climate warming. Here, we show through in situ and ex situ incubations that H2 consumption is an exceptionally thermally resilient process that can occur from -20 to +75{degrees}C, at rates comparable to temperate ecosystems (peaking at 8.56 nmol H2 h-1 g dry soil-1 at 25{degrees}C). Temperature ranges of CO (-20 to 42{degrees}C) and CH4 (-20 to 30{degrees}C) oxidation are also wider than expected, though the pattern of thermal sensitivity conforms with general theory. Metagenomic analyses support these data, revealing that atmospheric H2 and CO oxidisers are widespread, diverse, and abundant, and suggesting most Antarctic bacteria function below their temperature optima for these processes. Modelling of seasonal temperatures across ice-free Antarctica under current and future emissions scenarios indicates that H2 and CO oxidation can occur year-round, increasing by up to 35% or 44%, respectively, by 2100. Our results indicate constitutive aerotrophic activity contributing to Antarctic ecosystem functioning and biodiversity across spatial and temporal scales, with further studies required to understand how it interacts with photosynthesis in a changing climate.

microbiology↗

The economic strategies of superorganisms

The leaf economics spectrum links strategies of plant investment in resource-acquiring leaves to overall fitness. We test whether an economic spectrum can also explain variation in ecological strategies of ant species across environmental gradients, where colony investment in workers is analogous to plant investment in leaves. A fast return of resource investment was associated with large colonies of smaller, less robust, short-lived workers with low nitrogen:phosphorus ratios. Slow resource payback was associated with small colonies of densely built, energetically conservative and longer-lived workers with high nitrogen:phosphorus ratios. Species representing the entire economic continuum co-occurred in all communities. Phylogenetic analyses suggest genus level conservation of core investment templates. These results unify studies of plants and ants, suggesting common economic principles apply across the tree of life.

ecology↗

Antarctic biosecurity policy effectively manages the rates of alien introductions

Reducing the rates and impacts of biological invasions is a major policy goal of international biodiversity agreements. Yet the extent to which this goal is being achieved and the agreements hence successful in this respect remains unclear. Here we use a comprehensive record of alien species introduction in the terrestrial Antarctic, including its surrounding Southern Ocean Islands, spanning 115 years (1900-2015), to quantify the impact of biosecurity policy on alien species introduction rates in the region, where invasive alien species are a primary environmental conservation threat and management priority. We show that although many parts of the Antarctic have been colonised by non-indigenous taxa, recent rates of introduction appear to be slowing or static in most parts, compared with increases in the past. Our results vindicate the regional Antarctic focus on biosecurity measures, but also demonstrate the need for stricter enforcement due to rapid socio-environmental changes. Three key pointsO_LIBiological invasions present a large and growing threat to Antarctic ecosystems under climate change and expanding human activity C_LIO_LIOver the 20th century, there was no trend in alien species introduction rate in five Antarctic regions and a significantly increasing trend in the remaining five regions C_LIO_LIDespite this variation, in most regions, the number of introductions remains low, indicating that Antarctic biosecurity has been effective at slowing the rate of introduction C_LI

ecology↗

Global increase in the endemism of birds from north to south

Endemism is a highly valuable metric for conservation because it identifies areas with irreplaceable species, ecological functions, or evolutionary lineages1-6. Global analyses of endemism currently fail to identify the most irreplaceable areas because the commonly used endemism metrics are correlated with richness, and entire regions, especially in the southern hemisphere, are regularly excluded7-11. Global patterns of endemism are therefore still insufficiently known. Here, using metrics representing irreplaceability, we unveil global patterns of avian taxonomic, functional, and phylogenetic endemism that show striking differences between hemispheres. Across all facets of diversity, endemism decreases poleward in the northern, but increases poleward in the southern, hemisphere, resulting in a global north-south increase in endemism. The pattern is driven by increasingly smaller and discontinuous landmasses towards the south leading to increasingly smaller ranges and reduced overlap in community composition, and, unexpectedly, to peaks of diversity relative to available area in the southern hemisphere. The current misapprehension of global endemism potentially compromises urgent conservation actions, drawing attention away from key areas of irreplaceability. Highly endemic southern-hemisphere communities might be especially vulnerable to the climate crisis because discontinuous landmasses impede range shifts.

ecology↗

Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Most aerated cave ecosystems are assumed to be oligotrophic given they receive minimal inputs of light energy. Diverse microorganisms have nevertheless been detected within caves, though it remains unclear what strategies enable them to meet their energy and carbon needs. Here we determined the processes and mediators of primary production in aerated limestone and basalt caves through paired metagenomic and biogeochemical profiling. Based on 1458 metagenome-assembled genomes, over half of microbial cells in caves encode enzymes to use atmospheric trace gases as energy and carbon sources. The most abundant microbes in these systems are chemosynthetic primary producers, notably the novel gammaproteobacterial methanotrophic order Ca. Methylocavales and two uncultivated actinobacterial genera predicted to grow on atmospheric hydrogen, carbon dioxide, and carbon monoxide. In situ and ex situ biogeochemical and isotopic measurements consistently confirmed that these gases are rapidly consumed at rates sufficient to meet community-wide energy needs and drive continual primary production. Conventional chemolithoautotrophs, which use trace lithic compounds such as ammonium and sulfide, are also enriched and active alongside these trace gas scavengers. These results indicate that caves are unique in both their microbial composition and the biogeochemical processes that sustain them. Based on these findings, we propose caves are the first known ecosystems where atmospheric trace gases primarily sustain growth rather than survival and define this process as aerotrophy. Cave aerotrophy may be a hidden process supporting global biogeochemistry.

microbiology↗

No evidence for song evolution influencing speciation patterns in honeyeaters

Birdsongs are acoustic signals that can play a role in sexual selection. Despite the established role of birdsong in selection and reproductive isolation at microevolutionary scales, the macroevolutionary relationships between song evolution and clade diversification remain largely unexplored. We test the hypothesis that shifts in diversification influence rates of song evolution in honeyeaters, a diverse clade of songbirds restricted to Australasia. Using a song dataset for 163 honeyeater species, we identify lineage-specific shifts in diversification, and test the influence of these shifts on song evolution with state-dependent, relaxed, multivariate Brownian motion models. We also explore the underlying patterns of song evolution and phylogenetic signal of song. Shifts to lower rates of diversification are associated with lower rates of song evolution. This suggests the two factors are correlated, but is contrary to expectations that elevated rates of diversification will be associated with elevated rates of song evolution. We also found that song follows a punctuated mode of evolution, implying that birdsong has an important role in speciation events, although this signal likely erodes over time and is subject to phylogenetic constraints.

evolutionary biology↗

Body size shapes song in honeyeaters

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size, a consequence of both global effects such as climate change, and local effects such as habitat transformation, will substantially influence the nature of birdsong.

evolutionary biology↗

Spatio-temporal development of the urban heat island in a socioeconomically diverse tropical city

Urban heat islands, where temperatures are elevated relative to non-urban surrounds, are near-ubiquitous in cities globally. Yet, the magnitude and form of urban heat islands in the tropics, where heat has a large morbidity and mortality burden, is less well understood, especially for socioeconomically diverse communities such as those living in urban informal settlements. We utilised 29 years of Landsat satellite-derived surface temperature, corroborated by in situ measurements, to provide a detailed spatial and temporal assessment of urban heat islands in Makassar, Indonesia, a city that is representative of rapidly growing urban settlements across the tropics. We did so with explicit consideration of vulnerable communities living informally. Our analysis identified surface urban heat islands of up to 9.2 {degrees}C in long-urbanised parts of the city and 6.3 {degrees}C in informal settlements, the seasonal patterns of which were driven by change in non-urban areas rather than in urban areas themselves. In recently urbanised areas, the majority of urban heat island increase occurred before areas became 50% urbanised. As tropical cities continue to expand we expect that urban heat islands will develop quickly as land is urbanised, whereas the established heat island in long-urbanised areas will remain stable in response to city expansion. Green and blue space protect some informal settlements from the worst urban heat islands and maintenance of such space will be essential to mitigate the growing heat burden from urban expansion and anthropogenic climate change. We advocate for green space to be prioritised in urban planning, redevelopment and informal settlement upgrading programs, with consideration of the unique environmental and socioeconomic context of tropical cities. HighlightsO_LILong-term, fine-scale data are essential to understand the dynamics of urban heat C_LIO_LISurface heat islands reached 9.2 {degrees}C in the urban core, 6.3 {degrees}C in informal settlements C_LIO_LIIn situ data support the use of remote sensing for heat island characterisation C_LIO_LIThe majority of heat island growth occurred before land was 50% urbanised C_LIO_LIGreen and blue space can mitigate heat in informal settlements C_LI

ecology↗

Globally invariant metabolism but density-diversity mismatch in springtails

Soil life supports the functioning and biodiversity of terrestrial ecosystems1, 2. Springtails (Collembola) are among the most abundant soil animals regulating soil fertility and flow of energy through above- and belowground food webs3-5. However, the global distribution of springtail diversity and density, and how these relate to energy fluxes remains unknown. Here, using a global dataset collected from 2,470 sites, we estimate total soil springtail biomass at 29 Mt carbon (threefold higher than wild terrestrial vertebrates6) and record peak densities up to 2 million individuals per m{superscript 2} in the Arctic. Despite a 20-fold biomass difference between tundra and the tropics, springtail energy use (community metabolism) remains similar across the latitudinal gradient, owing to the increase in temperature. Neither springtail density nor community metabolism were predicted by local species richness, which was highest in the tropics, but comparably high in some temperate forests and even tundra. Changes in springtail activity may emerge from latitudinal gradients in temperature, predation7, 8, and resource limitation7, 9, 10 in soil communities. Contrasting temperature responses of biomass, diversity and activity of springtail communities suggest that climate warming will alter fundamental soil biodiversity metrics in different directions, potentially restructuring terrestrial food webs and affecting major soil functions.

ecology↗

TaqMan Array Cards enable monitoring of diverse enteric pathogens across environmental and host reservoirs

BackgroundMultiple bacteria, viruses, protists, and helminths cause enteric infections that greatly impact human health and wellbeing. These enteropathogens are transmitted via several pathways through human, animal, and environmental reservoirs. Individual quantitative PCR (qPCR) assays have been extensively used to detect enteropathogens within these types of samples, whereas the TaqMan Array Card (TAC) that allows simultaneous detection of multiple enteropathogens has only previously been validated in human clinical samples. MethodsHere, we performed a comprehensive double-blinded comparison of the performance of a custom TAC relative to standard qPCR for the detection of eight enteric targets, by using spiked samples, wastewater from Melbourne (Australia), and human, animal, and environmental samples from informal settlements in Suva, Fiji. FindingsBoth methods exhibited high and comparable specificity (TAC: 100%, qPCR: 94%), sensitivity (TAC: 92%; qPCR: 100%), and quantitation accuracy (TAC: 91%; qPCR: 99%) in non-inhibited sample matrices. PCR inhibitors substantially impacted detection via TAC, though this issue was alleviated by 10-fold sample dilution. Among samples from informal settlements, the two techniques were comparable for detection (89% agreement) and quantitation (R2 = 0.82). The TAC additionally included 38 other targets, enabling detection of diverse faecal pathogens and extensive environmental contamination that would be prohibitively labour intensive to assay by standard qPCR. InterpretationOverall, the two techniques produce comparable results across diverse sample types, with qPCR prioritising greater sensitivity and quantitation accuracy, and TAC trading small reductions in these for a cost-effective larger enteropathogen panel that enables a greater number of enteric pathogens to be analysed concurrently, which is beneficial given the abundance and variety of enteric pathogens in environments such as urban informal settlements. The ability to monitor multiple enteric pathogens across diverse reservoirs in turn allows better resolution of pathogen exposure pathways, and the design and monitoring of interventions to reduce pathogen load. FundingWellcome Trust Our Planet, Our Health program [OPOH grant 205222/Z/16/Z].

microbiology↗

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↗

Antarctica's wilderness has declined to the exclusion of biodiversity

Recent assessments of the biodiversity value of Earth's dwindling wilderness areas have emphasized the whole of Antarctica as a crucial wilderness in need of urgent protection. Whole-of-continent designations for Antarctic conservation remain controversial, however, because of widespread human impacts and frequently used provisions in Antarctic law for the designation of specially protected areas to conserve wilderness values, species and ecosystems. Here we investigate the extent to which Antarctica's wilderness encompasses its biodiversity. We assembled a comprehensive record of human activity on the continent (~ 2.7 million localities) and used it to identify unvisited areas [≥] 10 000 km2 (i.e. Antarctica's wilderness areas) and their representation of biodiversity. We show that, at best, 7 770 000 km2 of wilderness remains, covering 56.9% of the continent's surface area, however it captures few important biodiversity features. Important Bird Areas, ice-free Antarctic Conservation Biogeographic Regions crucial for biodiversity and areas with verified biodiversity records are largely excluded. Our results demonstrate that Antarcticas wilderness has already declined to the exclusion of much of its biodiversity. But that on a continent set aside as a natural reserve, increased regulation of human activity and urgent expansion of the Antarctic specially protected area network could feasibly reverse this trend.

ecology↗

A widespread thermodynamic effect, but maintenance of biological rates through space across life’s major domains

For over a century, temperature compensation (maintenance of biological rates with changing temperatures) has remained controversial. An alternative idea, that fitness is greater at higher temperatures (the thermodynamic effect), has gained increasing traction, and is being used to understand large-scale biodiversity responses to environmental change. Yet evidence in favour of each of these contrasting hypotheses continues to emerge. In consequence, the fundamental nature of organismal thermal responses and its implications remain unresolved. Here we investigate these ideas explicitly using a global dataset of 619 observations of four categories of organismal performance, spanning 14 phyla and 403 species. In agreement with both hypotheses, we show a positive relationship between the temperature of maximal performance rate (Topt) and environmental temperature (Tenv) for all traits. Next we demonstrate that relationships between Tenv and the temperature of maximal performance rate (Umax) are rarely significant and positive, as expected if a thermodynamic effect predominates. By contrast, a positive relationship between Topt and Umax is always present, but markedly weaker than theoretically predicted. These outcomes demonstrate that while some form of thermodynamic effect exists, ample scope is present for biochemical and physiological adaptation to thermal environments in the form of temperature compensation.

ecology↗