Antarctic Desert Soils Research Articles

Metal(loid)-resistant bacterial consortia with antimycotic properties increase tolerance of Chenopodium quinoa Wild. to metal(loid) stress

Bacteria associated with plants colonizing extreme environments in Chile (Atacama and Antarctic Desert soils) provide a model to study plant growth-promoting mechanisms that can be useful to improve the growth of crops such as Chenopodium quinoa Wild. (Amaranthaceae) growing under severe environmental conditions. This study aimed to determine the tolerance of extremophile rhizobacteria to multiple metal(loid)s and evaluate the effects of formulated consortia in seed germination and growth-promotion of C. quinoa. In our work, five rhizobacteria were isolated and classified into the bacteria genera Streptomyces, Bacillus, and Pseudomonas. The five bacteria showed optimum growth at 26 °C, pH 6, and 1% NaCl. In addition, the isolated were resistant to arsenic, manganese, zinc, copper, chromium and showed plant growth-promoting traits, including indole acetic acid production, siderophores production, phosphate solubilization, ACC deaminase activity, and ammonia production. According to compatibility tests, three bacterial consortia were formulated: i) consortium A (Pseudomonas sp. and Bacillus sp. (T1B41)); ii) consortium B (Pseudomonas sp. and Bacillus sp. (B2B24)); and iii) consortium C (Streptomyces sp., Bacillus sp. (B2B24) and Bacillus sp. (T3B45)). In vitro antagonism against phytopathogenic fungi showed that Bacillus sp. (B2B24) and Bacillus sp. (T3B45) have a significant level of antagonism (up to 18.7 and 6.8%, respectively) and consortia were the most effective against B. cinerea (up to 100%). Consortia B and C significantly improved the germination rate (%) of C. quinoa seeds (86 ± 3.3 and 77 ± 1.7, respectively) and the number of leaves, wet stem weight, length stem length, wet root weight, and root diameter in the presence of metal(loid)s. Our results showed that rhizobacterial consortia based on extremophile microorganisms can enhance the growth of C. quinoa seedlings under metal(loid) stress, demonstrating beneficial characteristics that may be key in the early stages of development.

Microbial oxidation of atmospheric trace gases.

The atmosphere has recently been recognized as a major source of energy sustaining life. Diverse aerobic bacteria oxidize the three most abundant reduced trace gases in the atmosphere, namely hydrogen (H2), carbon monoxide (CO) and methane (CH4). This Review describes the taxonomic distribution, physiological role and biochemical basis of microbial oxidation of these atmospheric trace gases, as well as the ecological, environmental, medical and astrobiological importance of this process. Most soil bacteria and some archaea can survive by using atmospheric H2 and CO as alternative energy sources, as illustrated through genetic studies on Mycobacterium cells and Streptomyces spores. Certain specialist bacteria can also grow on air alone, as confirmed by the landmark characterization of Methylocapsa gorgona, which grows by simultaneously consuming atmospheric CH4, H2 and CO. Bacteria use high-affinity lineages of metalloenzymes, namely hydrogenases, CO dehydrogenases and methane monooxygenases, to utilize atmospheric trace gases for aerobic respiration and carbon fixation. More broadly, trace gas oxidizers enhance the biodiversity and resilience of soil and marine ecosystems, drive primary productivity in extreme environments such as Antarctic desert soils and perform critical regulatory services by mitigating anthropogenic emissions of greenhouse gases and toxic pollutants.

Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils

Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse mountainous and glacial soils. We assembled 451 metagenome-assembled genomes from 18 microbial phyla and inferred through Bayesian divergence analysis that the dominant lineages present are likely native to Antarctica. In support of earlier findings, metagenomic analysis revealed that the most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen to support aerobic respiration and sometimes carbon fixation. Surprisingly, however, hydrogen oxidation in this region was catalyzed primarily by a phylogenetically and structurally distinct enzyme, the group 1l [NiFe]-hydrogenase, encoded by nine bacterial phyla. Through gas chromatography, we provide evidence that both Antarctic soil communities and an axenic Bacteroidota isolate (Hymenobacter roseosalivarius) oxidize atmospheric hydrogen using this enzyme. Based on ex situ rates at environmentally representative temperatures, hydrogen oxidation is theoretically sufficient for soil communities to meet energy requirements and, through metabolic water production, sustain hydration. Diverse carbon monoxide oxidizers and abundant methanotrophs were also active in the soils. We also recovered genomes of microorganisms capable of oxidizing edaphic inorganic nitrogen, sulfur, and iron compounds and harvesting solar energy via microbial rhodopsins and conventional photosystems. Obligately symbiotic bacteria, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also present. We conclude that microbial diversity in Antarctic soils reflects the coexistence of metabolically flexible mixotrophs with metabolically constrained specialists.

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.

Understanding the Response of Nitrifying Communities to Disturbance in the McMurdo Dry Valleys, Antarctica.

Polar ecosystems are generally limited in nitrogen (N) nutrients, and the patchy availability of N is partly determined by biological pathways, such as nitrification, which are carried out by distinctive prokaryotic functional groups. The activity and diversity of microorganisms are generally strongly influenced by environmental conditions. However, we know little of the attributes that control the distribution and activity of specific microbial functional groups, such as nitrifiers, in extreme cold environments and how they may respond to change. To ascertain relationships between soil geochemistry and the ecology of nitrifying microbial communities, we carried out a laboratory-based manipulative experiment to test the selective effect of key geochemical variables on the activity and abundance of ammonia-oxidizing communities in soils from the McMurdo Dry Valleys of Antarctica. We hypothesized that nitrifying communities, adapted to different environmental conditions within the Dry Valleys, will have distinct responses when submitted to similar geochemical disturbances. In order to test this hypothesis, soils from two geographically distant and geochemically divergent locations, Miers and Beacon Valleys, were incubated over 2 months under increased conductivity, ammonia concentration, copper concentration, and organic matter content. Amplicon sequencing of the 16S rRNA gene and transcripts allowed comparison of the response of ammonia-oxidizing Archaea (AOA) and ammonia-oxidizing Bacteria (AOB) to each treatment over time. This approach was combined with measurements of 15NH4+ oxidation rates using 15N isotopic additions. Our results showed a higher potential for nitrification in Miers Valley, where environmental conditions are milder relative to Beacon Valley. AOA exhibited better adaptability to geochemical changes compared to AOB, particularly to the increase in copper and conductivity. AOA were also the only nitrifying group found in Beacon Valley soils. This laboratorial manipulative experiment provided new knowledge on how nitrifying groups respond to changes on key geochemical variables of Antarctic desert soils, and we believe these results offer new insights on the dynamics of N cycling in these ecosystems.

DrwH, a novel WHy domain-containing hydrophobic LEA5C protein from Deinococcus radiodurans, protects enzymatic activity under oxidative stress

Water stress and hypersensitive response (WHy) domain is typically found as a component of atypical late embryogenesis abundant (LEA) proteins closely associated with resistance to multiple stresses in numerous organisms. Several putative LEA proteins have been identified in Deinococcus bacteria; however their precise function remains unclear. This work reports the characterization of a Deinococcus-specific gene encoding a novel WHy domain-containing hydrophobic LEA5C protein (named DrwH) in D. radiodurans R1. The expression of the drwH gene was induced by oxidative and salinity stresses. Inactivation of this gene resulted in increased sensitivity to oxidative and salinity stresses as well as reduced activities of antioxidant enzymes. The WHy domain of the DrwH protein differs structurally from that of a previously studied bacterial LEA5C protein, dWHy1, identified as a gene product from an Antarctic desert soil metagenome library. Further analysis indicated that in E. coli, the function of DrwH is related to oxidative stress tolerance, whereas dWHy1 is associated with freezing-thawing stress tolerance. Under oxidative stress induced by H2O2, DrwH protected the enzymatic activities of malate dehydrogenase (MDH) and lactate dehydrogenase (LDH). These findings provide new insight into the evolutionary and survival strategies of Deinococcus bacteria under extreme environmental conditions.

The genome of the Antarctic polyextremophile Nesterenkonia sp. AN1 reveals adaptive strategies for survival under multiple stress conditions.

Nesterenkonia sp. AN1 is a polyextremophile isolated from Antarctic desert soil. Genomic analyses and genome comparisons with three mesophilic Nesterenkonia strains indicated that the unique genome fraction of Nesterenkonia sp. AN1 contains adaptive features implicated in the response to cold stress including modulation of membrane fluidity as well as response to cold-associated osmotic and oxidative stress. The core genome also encodes a number of putative cold stress response proteins. RNA-Seq-based transcriptome analyses of Nesterenkonia sp. AN1 grown at 5ºC and 21°C showed that there was significant induction of transcripts that code for antioxidants at 5ºC, demonstrated by the upregulation of sodA, bcp and bpoA2. There was also overexpression of universal stress protein genes related to uspA, along with genes encoding other characterized cold stress features. Genes encoding the two key enzymes of the glyoxylate cycle, isocitrate lyase (ICL) and malate synthase (AceB) were induced at 5ºC, suggesting possible adaptation strategies for energy metabolism in cold habitats. These genomic features may contribute to the survival of Nesterenkonia sp. AN1 in arid Antarctic soils.

A novel bacterial Water Hypersensitivity-like protein shows in vivo protection against cold and freeze damage.

Metagenomic library screening, by functional or sequence analysis, has become an established method for the identification of novel genes and gene products, including genetic elements implicated in microbial stress response and adaptation. We have identified, using a sequence-based approach, a fosmid clone from an Antarctic desert soil metagenome library containing a novel gene which codes for a protein homologous to a Water Hypersensitivity domain (WHy). The WHy domain is typically found as a component of specific LEA (Late Embryogenesis Abundant) proteins, particularly the LEA-14 (LEA-8) variants, which occur widely in plants, nematodes, bacteria and archaea and which are typically induced by exposure to stress conditions. The novel WHy-like protein (165 amino acid, 18.6 kDa) exhibits a largely invariant NPN motif at the N-terminus and has high sequence identity to genes identified in Pseudomonas genomes. Expression of this protein in Escherichia coli significantly protected the recombinant host against cold and freeze stress.

Draft genomic DNA sequence of the multi-resistant Sphingomonas sp. strain AntH11 isolated from an Antarctic hypolith.

Hypoliths are microbial communities that live underneath translucent rocks in desert ecosystems and represent a key refuge niche in the Antarctic Dry Valleys. These cryptic microbial assemblages are crucial as they mediate numerous ecosystem processes. Here, we present the first draft genome of a hypolith isolate belonging to the α-proteobacterial class and the genus Sphingomonas. The draft genome of Sphingomonas sp. strain AntH11 shows the capacity of this organism to adapt to the extreme cold and arid conditions encountered in Antarctic desert soils. Our result also suggests that its metabolic versatility and multidrug resistance constitutes an opportunistic advantage in competition with other hypolith-colonizing microorganisms.

Microbial ecology and biogeochemistry of continental Antarctic soils.

The Antarctica Dry Valleys are regarded as the coldest hyperarid desert system on Earth. While a wide variety of environmental stressors including very low minimum temperatures, frequent freeze-thaw cycles and low water availability impose severe limitations to life, suitable niches for abundant microbial colonization exist. Antarctic desert soils contain much higher levels of microbial diversity than previously thought. Edaphic niches, including cryptic and refuge habitats, microbial mats and permafrost soils all harbor microbial communities which drive key biogeochemical cycling processes. For example, lithobionts (hypoliths and endoliths) possess a genetic capacity for nitrogen and carbon cycling, polymer degradation, and other system processes. Nitrogen fixation rates of hypoliths, as assessed through acetylene reduction assays, suggest that these communities are a significant input source for nitrogen into these oligotrophic soils. Here we review aspects of microbial diversity in Antarctic soils with an emphasis on functionality and capacity. We assess current knowledge regarding adaptations to Antarctic soil environments and highlight the current threats to Antarctic desert soil communities.

Draft Genome Sequence of Williamsia sp. Strain D3, Isolated From the Darwin Mountains, Antarctica

Actinobacteria are the dominant taxa in Antarctic desert soils. Here, we describe the first draft genome of a member of the genus Williamsia (strain D3) isolated from Antarctic soil. The genome of this psychrotolerant bacterium may help to elucidate crucial survival mechanisms for organisms inhabiting cold desert soil systems.

A novel, extremely alkaliphilic and cold-active esterase from Antarctic desert soil

A novel, cold-active and highly alkaliphilic esterase was isolated from an Antarctic desert soil metagenomic library by functional screening. The 1,044bp gene sequence contained several conserved regions common to lipases/esterases, but lacked clear classification based on sequence analysis alone. Moderate (<40%) amino acid sequence similarity to known esterases was apparent (the closest neighbour being a hypothetical protein from Chitinophaga pinensis), despite phylogenetic distance to many of the lipolytic "families". The enzyme functionally demonstrated activity towards shorter chain p-nitrophenyl esters with the optimal activity recorded towards p-nitrophenyl propionate (C3). The enzyme possessed an apparent T(opt) at 20°C and a pH optimum at pH 11. Esterases possessing such extreme alkaliphily are rare and so this enzyme represents an intriguing novel locus in protein sequence space. A metagenomic approach has been shown, in this case, to yield an enzyme with quite different sequential/structural properties to known lipases. It serves as an excellent candidate for analysis of the molecular mechanisms responsible for both cold and alkaline activity and novel structure-function relationships of esterase activity.

Hypolithic communities: important nitrogen sources in Antarctic desert soils

Hypolithic microbial communities (i.e. cryptic microbial assemblages found on the undersides of translucent rocks) are major contributors of carbon input into the oligotrophic hyper-arid desert mineral soils of the Eastern Antarctic Dry Valleys. Here we demonstrate, for the first time, that hypolithic microbial communities possess both the genetic capacity for nitrogen fixation (i.e. the presence of nifH genes) and the ability to catalyse acetylene reduction, an accepted proxy for dinitrogen fixation. An estimate of the total contribution of these communities suggests that hypolithic communities are important contributors to fixed nitrogen budgets in Antarctic desert soils.

Unique Aliphatic Amidase from a Psychrotrophic and Haloalkaliphilic Nesterenkonia Isolate

Nesterenkonia strain AN1 was isolated from a screening program for nitrile- and amide-hydrolyzing microorganisms in Antarctic desert soil samples. Strain AN1 showed significant 16S rRNA sequence identity to known members of the genus. Like known Nesterenkonia species, strain AN1 was obligately alkaliphilic (optimum environmental pH, 9 to 10) and halotolerant (optimum environmental Na(+) content, 0 to 15% [wt/vol]) but was also shown to be an obligate psychrophile with optimum growth at approximately 21°C. The partially sequenced genome of AN1 revealed an open reading frame (ORF) encoding a putative protein member of the nitrilase superfamily, referred to as NitN (264 amino acids). The protein crystallized readily as a dimer and the atomic structure of all but 10 amino acids of the protein was determined, confirming that the enzyme had an active site and a fold characteristic of the nitrilase superfamily. The protein was screened for activity against a variety of nitrile, carbamoyl, and amide substrates and was found to have only amidase activity. It had highest affinity for propionamide but demonstrated a low catalytic rate. NitN had maximal activity at 30°C and between pH 6.5 and 7.5, conditions which are outside the optimum growth range for the organism.

Identification of a Novel Alkaliphilic Esterase Active at Low Temperatures by Screening a Metagenomic Library from Antarctic Desert Soil

A novel esterase was identified through functional screening of a metagenomic library in Escherichia coli obtained from Antarctic desert soil. The 297-amino-acid sequence had only low (<29%) similarity to a putative esterase from Burkholderia xenovorans. The enzyme was active over a temperature range of 7 to 54 degrees C and at alkaline pH levels and is a potential candidate for industrial application.