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.

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.

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 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.

The ecological roles of microbial lipopeptides: Where are we going?

Lipopeptides (LPs) are secondary metabolites produced by a diversity of bacteria and fungi. Their unique chemical structure comprises both a peptide and a lipid moiety. LPs are of major biotechnological interest owing to their emulsification, antitumor, immunomodulatory, and antimicrobial activities. To date, these versatile compounds have been applied across multiple industries, from pharmaceuticals through to food processing, cosmetics, agriculture, heavy metal, and hydrocarbon bioremediation. The variety of LP structures and the diversity of the environments from which LP-producing microorganisms have been isolated suggest important functions in their natural environment. However, our understanding of the ecological role of LPs is limited. In this review, the mode of action and the role of LPs in motility, antimicrobial activity, heavy metals removal and biofilm formation are addressed. We include discussion on the need to characterise LPs from a diversity of microorganisms, with a focus on taxa inhabiting 'extreme' environments. We introduce the use of computational target fishing and molecular dynamics simulations as powerful tools to investigate the process of interaction between LPs and cell membranes. Together, these advances will provide new understanding of the mechanism of action of novel LPs, providing greater insights into the roles of LPs in the natural environment.

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.

Discovery of an Abundance of Biosynthetic Gene Clusters in Shark Bay Microbial Mats.

Microbial mats are geobiological multilayered ecosystems that have significant evolutionary value in understanding the evolution of early life on Earth. Shark Bay, Australia has some of the best examples of modern microbial mats thriving under harsh conditions of high temperatures, salinity, desiccation, and ultraviolet (UV) radiation. Microorganisms living in extreme ecosystems are thought to potentially encode for secondary metabolites as a survival strategy. Many secondary metabolites are natural products encoded by a grouping of genes known as biosynthetic gene clusters (BGCs). Natural products have diverse chemical structures and functions which provide competitive advantages for microorganisms and can also have biotechnology applications. In the present study, the diversity of BGC were described in detail for the first time from Shark Bay microbial mats. A total of 1477 BGCs were detected in metagenomic data over a 20 mm mat depth horizon, with the surface layer possessing over 200 BGCs and containing the highest relative abundance of BGCs of all mat layers. Terpene and bacteriocin BGCs were highly represented and their natural products are proposed to have important roles in ecosystem function in these mat systems. Interestingly, potentially novel BGCs were detected from Heimdallarchaeota and Lokiarchaeota, two evolutionarily significant archaeal phyla not previously known to possess BGCs. This study provides new insights into how secondary metabolites from BGCs may enable diverse microbial mat communities to adapt to extreme environments.

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.

Harnessing long-read amplicon sequencing to uncover NRPS and Type I PKS gene sequence diversity in polar desert soils.

The severity of environmental conditions at Earth's frigid zones present attractive opportunities for microbial biomining due to their heightened potential as reservoirs for novel secondary metabolites. Arid soil microbiomes within the Antarctic and Arctic circles are remarkably rich in Actinobacteria and Proteobacteria, bacterial phyla known to be prolific producers of natural products. Yet the diversity of secondary metabolite genes within these cold, extreme environments remain largely unknown. Here, we employed amplicon sequencing using PacBio RS II, a third generation long-read platform, to survey over 200 soils spanning twelve east Antarctic and high Arctic sites for natural product-encoding genes, specifically targeting non-ribosomal peptides (NRPS) and Type I polyketides (PKS). NRPS-encoding genes were more widespread across the Antarctic, whereas PKS genes were only recoverable from a handful of sites. Many recovered sequences were deemed novel due to their low amino acid sequence similarity to known protein sequences, particularly throughout the east Antarctic sites. Phylogenetic analysis revealed that a high proportion were most similar to antifungal and biosurfactant-type clusters. Multivariate analysis showed that soil fertility factors of carbon, nitrogen and moisture displayed significant negative relationships with natural product gene richness. Our combined results suggest that secondary metabolite production is likely to play an important physiological component of survival for microorganisms inhabiting arid, nutrient-starved soils.