Novel endolithic bacteria of phylum Chloroflexota reveal a myriad of potential survival strategies in the Antarctic desert.

The ice-free McMurdo Dry Valleys of Antarctica are dominated by nutrient-poor mineral soil and rocky outcrops. The principal habitat for microorganisms is within rocks (endolithic). In this environment, microorganisms are provided with protection against sub-zero temperatures, rapid thermal fluctuations, extreme dryness, and ultraviolet and solar radiation. Endolithic communities include lichen, algae, fungi, and a diverse array of bacteria. Chloroflexota is among the most abundant bacterial phyla present in these communities. Among the Chloroflexota are four novel classes of bacteria, here named Candidatus Spiritibacteria class. nov. (=UBA5177), Candidatus Martimicrobia class. nov. (=UBA4733), Candidatus Tarhunnaeia class. nov. (=UBA6077), and Candidatus Uliximicrobia class. nov. (=UBA2235). We retrieved 17 high-quality metagenome-assembled genomes (MAGs) that represent these four classes. Based on genome predictions, all these bacteria are inferred to be aerobic heterotrophs that encode enzymes for the catabolism of diverse sugars. These and other organic substrates are likely derived from lichen, algae, and fungi, as metabolites (including photosynthate), cell wall components, and extracellular matrix components. The majority of MAGs encode the capacity for trace gas oxidation using high-affinity uptake hydrogenases, which could provide energy and metabolic water required for survival and persistence. Furthermore, some MAGs encode the capacity to couple the energy generated from H2 and CO oxidation to support carbon fixation (atmospheric chemosynthesis). All encode mechanisms for the detoxification and efflux of heavy metals. Certain MAGs encode features that indicate possible interactions with other organisms, such as Tc-type toxin complexes, hemolysins, and macroglobulins.IMPORTANCEThe ice-free McMurdo Dry Valleys of Antarctica are the coldest and most hyperarid desert on Earth. It is, therefore, the closest analog to the surface of the planet Mars. Bacteria and other microorganisms survive by inhabiting airspaces within rocks (endolithic). We identify four novel classes of phylum Chloroflexota, and, based on interrogation of 17 metagenome-assembled genomes, we predict specific metabolic and physiological adaptations that facilitate the survival of these bacteria in this harsh environment-including oxidation of trace gases and the utilization of nutrients (including sugars) derived from lichen, algae, and fungi. We propose that such adaptations allow these endolithic bacteria to eke out an existence in this cold and extremely dry habitat.

Effects of increasing soil moisture on Antarctic desert microbial ecosystems.

Overgeneralization and a lack of baseline data for microorganisms in high-latitude environments have restricted the understanding of the microbial response to climate change, which is needed to establish Antarctic conservation frameworks. To bridge this gap, we examined over 17,000 sequence variants of bacteria and microeukarya across the hyperarid Vestfold Hills and Windmill Islands regions of eastern Antarctica. Using an extended gradient forest model, we quantified multispecies response to variations along 79 edaphic gradients to explore the effects of change and wind-driven dispersal on community dynamics under projected warming trends. We also analyzed a second set of soil community data from the Windmill Islands to test our predictions of major environmental tipping points. Soil moisture was the most robust predictor for shaping the regional soil microbiome; the highest rates of compositional turnover occurred at 10-12% soil moisture threshold for photoautotrophs, such as Cyanobacteria, Chlorophyta, and Ochrophyta. Dust profiles revealed a high dispersal propensity for Chlamydomonas, a microalga, and higher biomass was detected at trafficked research stations. This could signal the potential for algal blooms and increased nonendemic species dispersal as human activities increase in the region. Predicted increases in moisture availability on the Windmill Islands were accompanied by high photoautotroph abundances. Abundances of rare oligotrophic taxa, such as Eremiobacterota and Candidatus Dormibacterota, which play a crucial role in atmospheric chemosynthesis, declined over time. That photosynthetic taxa increased as soil moisture increased under a warming scenario suggests the potential for competition between primary production strategies and thus a more biotically driven ecosystem should the climate become milder. Better understanding of environmental triggers will aid conservation efforts, and it is crucial that long-term monitoring of our study sites be established for the protection of Antarctic desert ecosystems. Furthermore, the successful implementation of an improved gradient forest model presents an exciting opportunity to broaden its use on microbial systems globally.

Efectos del incremento de la humedad del suelo sobre los ecosistemas microbianos del desierto antártico Resumen La sobre generalización y la falta de datos de línea base de los microorganismos en los ambientes de latitudes elevadas han limitado el conocimiento de la respuesta microbiana al cambio climático, la cual es necesaria para establecer marcos de conservación en la Antártida. Para cerrar esta brecha analizamos más de 17,000 variantes de secuencias de bacterias y micro eucariontes de las regiones híper­áridas de las Colinas Vestfold y las Islas Windmill en el este de la Antártida. Usamos un modelo de gradiente de bosque extendido para cuantificar la respuesta de múltiples especies a la variación de 79 gradientes edáficos y así explorar los efectos del cambio y la dispersión eólica sobre las dinámicas comunitarias bajo las tendencias proyectadas de calentamiento. También analizamos un segundo conjunto de datos de la comunidad del suelo de las Islas Windmill para probar nuestras predicciones de los principales puntos de inflexión ambiental. La humedad del suelo fue el pronóstico más sólido para la composición del microbioma del suelo regional; las tasas más altas de rotación composicional ocurrieron con el 10­12% de humedad del suelo para los fotoautótrofos, como Cyanobacteria, Chlorophyta, y Ochrophyta. Los perfiles de polvo revelaron una alta tendencia de dispersión para Chlamydomonas, una microalga, y detectamos una biomasa más alta en las estaciones de investigación con tráfico. Esto podría significar un potencial para el brote de algas y un incremento en la dispersión de especies no endémicas conforme las actividades humanas incrementan en la región. El incremento pronosticado de la humedad disponible en las Islas Windmill estuvo acompañado de una abundancia elevada de fotoautótrofos. Hubo una declinación con el tiempo en la abundancia de taxones raros, como Eremiobacterota y Ca. Dormibacterota, las cuales tienen un papel importante en la síntesis química de la atmósfera. Que exista un incremento de taxones fotosintéticos junto con el incremento de la humedad del suelo bajo un escenario de calentamiento sugiere un potencial de competencia entre las estrategias primarias de producción, y por lo tanto un ecosistema con más factores bióticos, si es que el clima se vuelve más templado. Un mejor entendimiento de los detonadores ambientales ayudará a los esfuerzos de conservación, además que es importante que se establezca el monitoreo a largo plazo de nuestros sitios de estudio para la protección de los ecosistemas del desierto de la Antártida. Más aún, la implementación exitosa de un modelo de gradiente de bosque mejorado representa una oportunidad emocionante para ampliar su uso en los sistemas microbianos de mundo.

Atmospheric trace gases support primary production in Antarctic desert surface soil.

Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities. Given that phototroph abundance varies across these Antarctic soils, an enduring question is what supports life in those communities with low photosynthetic capacity. Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities. We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation. Soil microcosms aerobically scavenged atmospheric H2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO2 fixation. We propose that atmospheric H2, CO2 and CO provide dependable sources of energy and carbon to support these communities, which suggests that atmospheric energy sources can provide an alternative basis for ecosystem function to solar or geological energy sources. Although more extensive sampling is required to verify whether this process is widespread in terrestrial Antarctica and other oligotrophic habitats, our results provide new understanding of the minimal nutritional requirements for life and open the possibility that atmospheric gases support life on other planets.

Soil substrate culturing approaches recover diverse members of Actinomycetota from desert soils of Herring Island, East Antarctica.

Antimicrobial resistance is an escalating health crisis requiring urgent action. Most antimicrobials are natural products (NPs) sourced from Actinomycetota, particularly the Streptomyces. Underexplored and extreme environments are predicted to harbour novel microorganisms with the capacity to synthesise unique metabolites. Herring Island is a barren and rocky cold desert in East Antarctica, remote from anthropogenic impact. We aimed to recover rare and cold-adapted NP-producing bacteria, by employing two culturing methods which mimic the natural environment: direct soil culturing and the soil substrate membrane system. First, we analysed 16S rRNA gene amplicon sequencing data from 18 Herring Island soils and selected the soil sample with the highest Actinomycetota relative abundance (78%) for culturing experiments. We isolated 166 strains across three phyla, including novel and rare strains, with 94% of strains belonging to the Actinomycetota. These strains encompassed thirty-five 'species' groups, 18 of which were composed of Streptomyces strains. We screened representative strains for genes which encode polyketide synthases and non-ribosomal peptide synthetases, indicating that 69% have the capacity to synthesise polyketide and non-ribosomal peptide NPs. Fourteen Streptomyces strains displayed antimicrobial activity against selected bacterial and yeast pathogens using an in situ assay. Our results confirm that the cold-adapted bacteria of the harsh East Antarctic deserts are worthy targets in the search for bioactive compounds.

Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient-poor Antarctic soils.

Candidatus Dormibacterota is an uncultured bacterial phylum found predominantly in soil that is present in high abundances within cold desert soils. Here, we interrogate nine metagenome-assembled genomes (MAGs), including six new MAGs derived from soil metagenomes obtained from two eastern Antarctic sites. Phylogenomic and taxonomic analyses revealed these MAGs represent four genera and five species, representing two order-level clades within Ca. Dormibacterota. Metabolic reconstructions of these MAGs revealed the potential for aerobic metabolism, and versatile adaptations enabling persistence in the 'extreme' Antarctic environment. Primary amongst these adaptations were abilities to scavenge atmospheric H2 and CO as energy sources, as well as using the energy derived from H2 oxidation to fix atmospheric CO2 via the Calvin-Bassham-Benson cycle, using a RuBisCO type IE. We propose that these allow Ca. Dormibacterota to persist using H2 oxidation and grow using atmospheric chemosynthesis in terrestrial Antarctica. Fluorescence in situ hybridization revealed Ca. Dormibacterota to be coccoid cells, 0.3-1.4 µm in diameter, with some cells exhibiting the potential for a symbiotic or syntrophic lifestyle.

Antarctic desert soil bacteria exhibit high novel natural product potential, evaluated through long-read genome sequencing and comparative genomics.

Actinobacteria and Proteobacteria are important producers of bioactive natural products (NP), and these phyla dominate in the arid soils of Antarctica, where metabolic adaptations influence survival under harsh conditions. Biosynthetic gene clusters (BGCs) which encode NPs, are typically long and repetitious high G + C regions difficult to sequence with short-read technologies. We sequenced 17 Antarctic soil bacteria from multi-genome libraries, employing the long-read PacBio platform, to optimize capture of BGCs and to facilitate a comprehensive analysis of their NP capacity. We report 13 complete bacterial genomes of high quality and contiguity, representing 10 different cold-adapted genera including novel species. Antarctic BGCs exhibited low similarity to known compound BGCs (av. 31%), with an abundance of terpene, non-ribosomal peptide and polyketide-encoding clusters. Comparative genome analysis was used to map BGC variation between closely related strains from geographically distant environments. Results showed the greatest biosynthetic differences to be in a psychrotolerant Streptomyces strain, as well as a rare Actinobacteria genus, Kribbella, while two other Streptomyces spp. were surprisingly similar to known genomes. Streptomyces and Kribbella BGCs were predicted to encode antitumour, antifungal, antibacterial and biosurfactant-like compounds, and the synthesis of NPs with antibacterial, antifungal and surfactant properties was confirmed through bioactivity assays.

Distinct assembly mechanisms underlie similar biogeographical patterns of rare and abundant bacteria in Tibetan Plateau grassland soils.

Rare biosphere represents the majority of Earth's biodiversity and performs vital ecological functions, yet little is known about its biogeographical patterns and community assembly processes in terrestrial ecosystems. Herein, we investigated the community composition and phylogeny of rare (relative abundance <0.1%) and abundant (>1%) bacteria in dryland grassland soils on the Tibetan Plateau. Results revealed similar biogeographical patterns of rare and abundant bacteria at both compositional and phylogenetic levels, but rare subcommunity was more heavily influenced by stochasticity (72%) than the abundant (57%). The compositional variation of rare bacteria was less explained by environmental factors (41%) than that of the abundant (80%), while the phylogeny of rare bacteria (36%) was more explained than that of the abundant (29%). The phylogeny of rare bacteria was equally explained by local factors (soil and vegetation) and geospatial distance (11.5% and 11.9% respectively), while that of the abundant was more explained by geospatial distance (22.1%) than local factors (11.3%). Furthermore, a substantially tighter connection between the community phylogeny and composition was observed in rare (R2 = 0.65) than in abundant bacteria (R2 = 0.08). Our study provides novel insights into the assembly processes and biographical patterns of rare and abundant bacteria in dryland soils.

Communication within East Antarctic Soil Bacteria.

Antarctica, being the coldest, driest, and windiest continent on Earth, represents the most extreme environment in which a living organism can survive. Under constant exposure to harsh environmental threats, terrestrial Antarctica remains home to a great diversity of microorganisms, indicating that the soil bacteria must have adapted a range of survival strategies that require cell-to-cell communication. Survival strategies include secondary metabolite production, biofilm formation, bioluminescence, symbiosis, conjugation, sporulation, and motility, all of which are often regulated by quorum sensing (QS), a type of bacterial communication. Until now, such mechanisms have not been explored in terrestrial Antarctica. In this study, LuxI/LuxR-based quorum sensing (QS) activity was delineated in soil bacterial isolates recovered from Adams Flat, in the Vestfold Hills region of East Antarctica. Interestingly, we identified the production of potential homoserine lactones (HSLs) with chain lengths ranging from medium to long in 19 bacterial species using three biosensors, namely, Agrobacterium tumefaciens NTL4, Chromobacterium violaceum CV026, and Escherichia coli MT102, in conjunction with thin-layer chromatography (TLC). The majority of detectable HSLs were from Gram-positive species not previously known to produce HSLs. This discovery further expands our understanding of the microbial community capable of this type of communication, as well as provides insights into physiological adaptations of microorganisms that allow them to survive in the harsh Antarctic environment.IMPORTANCE Quorum sensing, a type of bacterial communication, is widely known to regulate many processes, including those that confer a survival advantage. However, little is known about communication by bacteria residing within Antarctic soils. Employing a combination of bacterial biosensors, analytical techniques, and genome mining, we found a variety of Antarctic soil bacteria speaking a common language, via LuxI/LuxR-based quorum sensing, thus potentially supporting survival in a mixed microbial community. This study reports potential quorum sensing activity in Antarctic soils and has provided a platform for studying physiological adaptations of microorganisms that allow them to survive in the harsh Antarctic environment.

Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale.

The current theoretical framework suggests that tripartite positive feedback relationships between soil biodiversity, fertility and plant productivity are universal. However, empirical evidence for these relationships at the continental scale and across different soil depths is lacking. We investigate the continental-scale relationships between the diversity of microbial and invertebrate-based soil food webs, fertility and above-ground plant productivity at 289 sites and two soil depths, that is 0-10 and 20-30 cm, across Australia. Soil biodiversity, fertility and plant productivity are strongly positively related in surface soils. Conversely, in the deeper soil layer, the relationships between soil biodiversity, fertility and plant productivity weaken considerably, probably as a result of a reduction in biodiversity and fertility with depth. Further modeling suggested that strong positive associations among soil biodiversity-fertility and fertility-plant productivity are limited to the upper soil layer (0-10 cm), after accounting for key factors, such as distance from the equator, altitude, climate and physicochemical soil properties. These findings highlight the importance of surface soil biodiversity for soil fertility, and suggest that any loss of surface soil could potentially break the links between soil biodiversity-fertility and/or fertility-plant productivity, which can negatively impact nutrient cycling and food production, upon which future generations depend.

Izhakiella australiensis sp. nov. isolated from an Australian desert soil.

A Gram-stain-negative, rod-shaped, non-motile bacterium, designated D4N98T, was isolated from a desert soil near Glendambo, Australia. The taxonomic position of strain D4N98T was investigated using a polyphasic approach. Strain D4N98T shared 97 % 16S rRNA gene sequence similarity with the only reference strain of the genus Izhakiella (Izhakiella capsodis N6PO6T), and less than 96 % similarity with other species of genera in the family Enterobacteriaceae with validly published names. Phylogenetic analysis, based on 16S rRNA, rpoB, atpD, gyrB genes and a concatenated sequence comprising 37 single copy marker genes, as well as chemotaxonomic data (major polar lipids: phosphatidyl ethanolamine, phosphatidylglycerol, diphosphatidylglycerol, a neutral lipid, and a glycolipid. Major fatty acids (>10 %): C16 : 0, C17 : 0 cyclo, summed feature 2 (C14 : 0 3-OH and/or iso-C16 : 1 I), summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c), summed feature 8 (C18 : 1ω7c and/or C18 : 1ω6c) support the affiliation of this strain to the genus Izhakiella. The results of in silico DNA-DNA hybridisation plus physiological and biochemical tests allowed genotypic and phenotypic differentiation of strain D4N98T from the other species of the genus Izhakiellawith validly published names. Therefore, strain D4N98T represents a novel species, for which the name Izhakiella australiensis sp. nov. is proposed. The type strain is D4N98T (LMG 30066T=DSM 105030T).

Specific global responses to N and Fe nutrition in toxic and non-toxic Microcystis aeruginosa.

The bloom-forming cyanobacteria species Microcystis aeruginosa includes toxic and non-toxic (microcystin-producing) strains. Certain stress conditions stimulate synthesis of microcystin (MCYST) and enhance the binding of the MCYST molecule to proteins. In this quantitative proteomic study, we compared the response of a wild-type toxic strain PCC 7806, an mcyH(-) knockout non-toxic strain, and a naturally occurring non-toxic strain, PCC 7005, after 8 days in low iron (Fe) and nitrogen (N) starvation in order to assess the benefit of MCYST synthesis in non-optimal conditions. Fe limitation increased MCYST synthesis and caused an accumulation of phycobilisome proteins and the ferric iron transporter FutA only in the toxic PCC 7806 but not the non-toxic strains. In N starvation, photosynthetic, C and N metabolism proteins were more abundant in the non-toxic strains, as were chaperones and proteases. Significant interaction between nutrient availability and toxicity existed for thioredoxin peroxidase and several thioredoxin-regulated proteins. We propose a competition of MCYST for binding sites in thioredoxin-regulated proteins during oxidative stress (low Fe) but not in growth-limiting conditions (low N). This then leads to differences in the regulation of C:N metabolism in toxic and non-toxic M. aeruginosa in nutrient-replete and nutrient-limited conditions.

Geological connectivity drives microbial community structure and connectivity in polar, terrestrial ecosystems.

Landscape heterogeneity impacts community assembly in animals and plants, but it is not clear if this ecological concept extends to microbes. To examine this question, we chose to investigate polar soil environments from the Antarctic and Arctic, where microbes often form the major component of biomass. We examined soil environments that ranged in connectivity from relatively well-connected slopes to patchy, fragmented landforms that comprised isolated frost boils. We found landscape connectedness to have a significant correlation with microbial community structure and connectivity, as measured by co-occurrence networks. Soils from within fragmented landforms appeared to exhibit less local environmental heterogeneity, harboured more similar communities, but fewer biological associations than connected landforms. This effect was observed at both poles, despite the geographical distances and ecological differences between them. We suggest that microbial communities inhabiting well-connected landscape elements respond consistently to regional-scale gradients in biotic and edaphic factors. Conversely, the repeated freeze thaw cycles that characterize fragmented landscapes create barriers within the landscape and act to homogenize the soil environment within individual frost boils and consequently the microbial communities. We propose that lower microbial connectivity in the fragmented landforms is a function of smaller patch size and continual disturbances following soil mixing.

Bacterial targets as potential indicators of diesel fuel toxicity in subantarctic soils.

Appropriate remediation targets or universal guidelines for polar regions do not currently exist, and a comprehensive understanding of the effects of diesel fuel on the natural microbial populations in polar and subpolar soils is lacking. Our aim was to investigate the response of the bacterial community to diesel fuel and to evaluate if these responses have the potential to be used as indicators of soil toxicity thresholds. We set up short- and long-exposure tests across a soil organic carbon gradient. Utilizing broad and targeted community indices, as well as functional genes involved in the nitrogen cycle, we investigated the bacterial community structure and its potential functioning in response to special Antarctic blend (SAB) diesel fuel. We found the primary effect of diesel fuel toxicity was a reduction in species richness, evenness, and phylogenetic diversity, with the resulting community heavily dominated by a few species, principally Pseudomonas. The decline in richness and phylogenetic diversity was linked to disruption of the nitrogen cycle, with species and functional genes involved in nitrification significantly reduced. Of the 11 targets we evaluated, we found the bacterial amoA gene indicative of potential ammonium oxidation, the most suitable indicator of toxicity. Dose-response modeling for this target generated an average effective concentration responsible for 20% change (EC20) of 155 mg kg(-1), which is consistent with previous Macquarie Island ecotoxicology assays. Unlike traditional single-species tolerance testing, bacterial targets allowed us to simultaneously evaluate more than 1,700 species from 39 phyla, inclusive of rare, sensitive, and functionally relevant portions of the community.

Metagenomics untangles potential adaptations of Antarctic endolithic bacteria at the fringe of habitability.

Survival and growth strategies of Antarctic endolithic microbes residing in Earth's driest and coldest desert remain virtually unknown. From 109 endolithic microbiomes, 4539 metagenome-assembled genomes were generated, 49.3 % of which were novel candidate bacterial species. We present evidence that trace gas oxidation and atmospheric chemosynthesis may be the prevalent strategies supporting metabolic activity and persistence of these ecosystems at the fringe of life and the limits of habitability.

Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa.

Toxin production in algal blooms presents a significant problem for the water industry. Of particular concern is microcystin, a potent hepatotoxin produced by the unicellular freshwater species Microcystis aeruginosa. In this study, the proteomes of six toxic and nontoxic strains of M. aeruginosa were analyzed to gain further knowledge in elucidating the role of microcystin production in this microorganism. This represents the first comparative proteomic study in a cyanobacterial species. A large diversity in the protein expression profiles of each strain was observed, with a significant proportion of the identified proteins appearing to be strain-specific. In total, 475 proteins were identified reproducibly and of these, 82 comprised the core proteome of M. aeruginosa. The expression of several hypothetical and unknown proteins, including four possible operons was confirmed. Surprisingly, no proteins were found to be produced only by toxic or nontoxic strains. Quantitative proteome analysis using the label-free normalized spectrum abundance factor approach revealed nine proteins that were differentially expressed between toxic and nontoxic strains. These proteins participate in carbon-nitrogen metabolism and redox balance maintenance and point to an involvement of the global nitrogen regulator NtcA in toxicity. In addition, the switching of a previously inactive toxin-producing strain to microcystin synthesis is reported.

Utilization of-Omic technologies in cold climate hydrocarbon bioremediation: a text-mining approach.

Hydrocarbon spills in cold climates are a prominent and enduring form of anthropogenic contamination. Bioremediation is one of a suite of remediation tools that has emerged as a cost-effective strategy for transforming these contaminants in soil, ideally into less harmful products. However, little is understood about the molecular mechanisms driving these complex, microbially mediated processes. The emergence of -omic technologies has led to a revolution within the sphere of environmental microbiology allowing for the identification and study of so called 'unculturable' organisms. In the last decade, -omic technologies have emerged as a powerful tool in filling this gap in our knowledge on the interactions between these organisms and their environment in vivo. Here, we utilize the text mining software Vosviewer to process meta-data and visualize key trends relating to cold climate bioremediation projects. The results of text mining of the literature revealed a shift over time from optimizing bioremediation experiments on the macro/community level to, in more recent years focusing on individual organisms of interest, interactions within the microbiome and the investigation of novel metabolic degradation pathways. This shift in research focus was made possible in large part by the rise of omics studies allowing research to focus not only what organisms/metabolic pathways are present but those which are functional. However, all is not harmonious, as the development of downstream analytical methods and associated processing tools have outpaced sample preparation methods, especially when dealing with the unique challenges posed when analyzing soil-based samples.

Clearing the air: unraveling past and guiding future research in atmospheric chemosynthesis.

SUMMARY: Atmospheric chemosynthesis is a recently proposed form of chemoautotrophic microbial primary production. The proposed process relies on the oxidation of trace concentrations of hydrogen (≤530 ppbv), carbon monoxide (≤90 ppbv), and methane (≤1,870 ppbv) gases using high-affinity enzymes. Atmospheric hydrogen and carbon monoxide oxidation have been primarily linked to microbial growth in desert surface soils scarce in liquid water and organic nutrients, and low in photosynthetic communities. It is well established that the oxidation of trace hydrogen and carbon monoxide gases widely supports the persistence of microbial communities in a diminished metabolic state, with the former potentially providing a reliable source of metabolic water. Microbial atmospheric methane oxidation also occurs in oligotrophic desert soils and is widespread throughout copiotrophic environments, with established links to microbial growth. Despite these findings, the direct link between trace gas oxidation and carbon fixation remains disputable. Here, we review the supporting evidence, outlining major gaps in our understanding of this phenomenon, and propose approaches to validate atmospheric chemosynthesis as a primary production process. We also explore the implications of this minimalistic survival strategy in terms of nutrient cycling, climate change, aerobiology, and astrobiology.

Out of Thin Air? Astrobiology and Atmospheric Chemotrophy.

The emerging understanding of microbial trace gas chemotrophy as a metabolic strategy to support energy and carbon acquisition for microbial survival and growth has significant implications in the search for past, and even extant, life beyond Earth. The use of trace gases, including hydrogen and carbon monoxide as substrates for microbial oxidation, potentially offers a viable strategy with which to support life on planetary bodies that possess a suitable atmospheric composition, such as Mars and Titan. Here, we discuss the current state of knowledge of this process and explore its potential in the field of astrobiological exploration.

Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts.

Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, bacterial primary production is supported by trace gas oxidation and the light-independent RuBisCO form IE. This study aims to determine if atmospheric chemosynthesis is widespread within Antarctic, Arctic and Tibetan cold deserts, to identify the breadth of trace gas chemosynthetic taxa and to further characterize the genetic determinants of this process. H2 oxidation was ubiquitous, far exceeding rates reported to fulfill the maintenance needs of similarly structured edaphic microbiomes. Atmospheric chemosynthesis occurred globally, contributing significantly (p < 0.05) to carbon fixation in Antarctica and the high Arctic. Taxonomic and functional analyses were performed upon 18 cold desert metagenomes, 230 dereplicated medium-to-high-quality derived metagenome-assembled genomes (MAGs) and an additional 24,080 publicly available genomes. Hydrogenotrophic and carboxydotrophic growth markers were widespread. RuBisCO IE was discovered to co-occur alongside trace gas oxidation enzymes in representative Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota genomes. We identify a novel group of high-affinity [NiFe]-hydrogenases, group 1m, through phylogenetics, gene structure analysis and homology modeling, and reveal substantial genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity 1h and 1l [NiFe]-hydrogenase groups. We conclude that atmospheric chemosynthesis is a globally-distributed phenomenon, extending throughout cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental reservoirs.