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.

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.

The Vestfold Hills are alive: characterising microbial and environmental dynamics in Old Wallow, eastern Antarctica.

Old Wallow is an underexplored, hyper-arid coastal desert in Antarctica's Vestfold Hills. Situated near an elephant seal wallow, we examined how stochastic nutrient inputs from the seal wallow affect soil communities amid environmental changes along a spatially explicit sampling transect. We hypothesized that nutrient levels would be elevated due to proximity to the seal wallow, influencing community distributions. While the soil bacterial and eukaryotic communities at the phylum level were similar to other terrestrial environments, analysis at class and family levels revealed a dominance of unclassified taxa that are often linked to marine environments. Elevated nutrient concentrations (NO3 -, SO4 2-, SO3) were found at Old Wallow, with conductivity and Cl- levels up to 10-fold higher at the lowest elevation soils, correlating with significantly (p < 0.05) higher abundances of halophilic (Halomonadaceace) and uncultivated lineages (Ca Actinomarinales, unclassified Bacillariophyta and unclassified Opisthonkonta). An improved Gradient Forest model was used to quantify microbial responses to 26 soil gradients at OW, revealing variable responses to environmental predictors and identifying critical environmental thresholds or drivers of community turnover. Major tipping points were projected for eukaryotes with SO4 2-, pH, and SO3, and for bacteria with moisture, Na2O, and Cl-. Thus, the Old Wallow ecosystem is primarily shaped by salt, sulphate, and moisture and is dominated by uncultivated taxa, which may be sensitive to environmental changes once critical tipping points are reached. This study provides critical baseline data for future regional monitoring under threats of environmental change.

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.

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.

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.

Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation.

Soil microbiomes within oligotrophic cold deserts are extraordinarily diverse. Increasingly, oligotrophic sites with low levels of phototrophic primary producers are reported, leading researchers to question their carbon and energy sources. A novel microbial carbon fixation process termed atmospheric chemosynthesis recently filled this gap as it was shown to be supporting primary production at two Eastern Antarctic deserts. Atmospheric chemosynthesis uses energy liberated from the oxidation of atmospheric hydrogen to drive the Calvin-Benson-Bassham (CBB) cycle through a new chemotrophic form of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), designated IE. Here, we propose that the genetic determinants of this process; RuBisCO type IE (rbcL1E) and high affinity group 1h-[NiFe]-hydrogenase (hhyL) are widespread across cold desert soils and that this process is linked to dry and nutrient-poor environments. We used quantitative PCR (qPCR) to quantify these genes in 122 soil microbiomes across the three poles; spanning the Tibetan Plateau, 10 Antarctic and three high Arctic sites. Both genes were ubiquitous, being present at variable abundances in all 122 soils examined (rbcL1E, 6.25 × 103-1.66 × 109 copies/g soil; hhyL, 6.84 × 103-5.07 × 108 copies/g soil). For the Antarctic and Arctic sites, random forest and correlation analysis against 26 measured soil physicochemical parameters revealed that rbcL1E and hhyL genes were associated with lower soil moisture, carbon and nitrogen content. While further studies are required to quantify the rates of trace gas carbon fixation and the organisms involved, we highlight the global potential of desert soil microbiomes to be supported by this new minimalistic mode of carbon fixation, particularly throughout dry oligotrophic environments, which encompass more than 35% of the Earth's surface.