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.

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.

Urea amendment decouples nitrification in hydrocarbon contaminated Antarctic soil.

Hydrocarbon contaminated soils resulting from human activities pose a risk to the natural environment, including in the Arctic and Antarctic. Engineered biopiles constructed at Casey Station, Antarctica, have proven to be an effective strategy for remediating hydrocarbon contaminated soils, with active ex-situ remediation resulting in significant reductions in hydrocarbons, even in the extreme Antarctic climate. However, the use of urea-based fertilisers, whilst providing a nitrogen source for bioremediation, has also altered the natural soil chemistry leading to increases in pH, ammonium and nitrite. Monitoring of the urea amended biopiles identified rising levels of nitrite to be of particular interest, which misaligns with the long term goal of reducing contaminant levels and returning soil communities to a 'healthy' state. Here, we combine amplicon sequencing, microfluidic qPCR on field samples and laboratory soil microcosms to assess the impact of persistent nitrite accumulation (up to 60 months) on nitrifier abundances observed within the Antarctic biopiles. Differential inhibition of ammonia oxidizing bacteria (AOB) and nitrite oxidizing bacteria (NOB) Nitrobacter and Nitrospira in the cold, urea treated, alkaline soils (pH 8.1) was associated with extensive nitrite accumulation (76 ± 57 mg N/kg at 60 months). When the ratio of Nitrospira:AOB dropped below ∼1:1, Nitrobacter was completely inhibited or absent from the biopiles, and nitrite accumulated. Laboratory soil microcosms (incubated at 7 °C and 15 °C for 9 weeks) reproduced the pattern of nitrite accumulation in urea fertilized soil at the lower temperature, consistent with our longer-term observations from the Antarctic biopiles, and with other temperature-controlled microcosm studies. Diammonium phosphate amended soil did not exhibit nitrite accumulation, and could be a suitable alternative biostimulant to avoid excessive nitrite build-up.

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.