Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities 1-3 . Given that phototroph abundance varies across these Antarctic soils 2,4 , an enduring question is what supports life in those communities with low photosynthetic capacity 3,5 . 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 6,7 . Soil microcosms aerobically scavenged atmospheric H 2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO 2 fixation. We propose that atmospheric H 2 , CO 2 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 8,9 . 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.Terrestrial Antarctica is among the most extreme environments on Earth. Its inhabitants experience the cumulative stresses of freezing temperatures, limited carbon, nitrogen and water availability, strong UV radiation, and frequent freeze-thaw cycles 2,10,11 . Although it was once believed that these conditions restrict life, we now know that the continent hosts a surprising diversity of macrofauna and microbiota 1,2,12 . Surveys indicate that the phylum-level composition of microbial communities in Antarctic soils is similar to those of temperate soils 3 , but Antarctic communities are highly specialized at the species level and strongly structured by physicochemical factors 1,3,10 . In many Antarctic soils, microorganisms are thought to live in dormant states 2 , with metabolic energy directed towards cell maintenance rather than growth 13 . However, it is unclear how these communities obtain the energy and carbon needed for maintenance, given that these soils are often low in organic carbon and contain few classical primary producers 2,5 .
Most aerobic bacteria exist in dormant states within natural environments. In these states, they endure adverse environmental conditions such as nutrient starvation by decreasing metabolic expenditure and using alternative energy sources. In this study, we investigated the energy sources that support persistence of two aerobic thermophilic strains of the environmentally widespread but understudied phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain upon entry into stationary phase due to nutrient limitation. Whereas primary dehydrogenases associated with heterotrophic respiration were downregulated, putative operons encoding enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H2 and CO at a range of environmentally relevant concentrations to sub-atmospheric levels. Phylogenetic analysis suggests that the hydrogenases and carbon monoxide dehydrogenases mediating these processes are widely distributed in Chloroflexi genomes and have probably been horizontally acquired on more than one occasion. Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence, though further studies are required to determine if these findings extend to mesophilic strains. This study provides axenic culture evidence that atmospheric CO supports bacterial persistence and reports the third phylum, following Actinobacteria and Acidobacteria, to be experimentally shown to mediate the biogeochemically and ecologically important process of atmospheric H2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.
Ecological theory suggests that habitat disturbance differentially influences distributions of habitat generalist and specialist species. While well-established for macroorganisms, this theory has rarely been explored for microorganisms. Here we tested these principles in permeable (sandy) sediments, ecosystems with much spatiotemporal variation in resource availability and physicochemical conditions. Microbial community composition and function were profiled in intertidal and subtidal sediments using 16S rRNA gene amplicon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Community composition and metabolic traits modestly varied with sediment depth and sampling date. Several taxa were highly abundant and prevalent in all samples, including within the orders Woeseiales and Flavobacteriales, and classified as habitat generalists; genome reconstructions indicate these taxa are highly metabolically flexible facultative anaerobes and adapt to resource variability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers and candidate lineage MBNT15 were less abundant overall and only thrived in more stable deeper sediments. We substantiated these findings by measuring three metabolic processes in these sediments; whereas the habitat generalist-associated processes of sulfide oxidation and fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. A manipulative experiment also confirmed habitat generalists outcompete specialist taxa during simulated habitat disturbance. Together, these findings show metabolically flexible habitat generalists become dominant in highly dynamic environments, whereas metabolically constrained specialists are restricted to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.
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.
Microbial life is surprisingly abundant and diverse in global desert ecosystems. In these environments, microorganisms endure a multitude of physicochemical stresses, including low water potential, carbon and nitrogen starvation, and extreme temperatures. In this review, we summarize our current understanding of the energetic mechanisms and trophic dynamics that underpin microbial function in desert ecosystems. Accumulating evidence suggests that dormancy is a common strategy that facilitates microbial survival in response to water and carbon limitation. Whereas photoautotrophs are restricted to specific niches in extreme deserts, metabolically versatile heterotrophs persist even in the hyper-arid topsoils of the Atacama Desert and Antarctica. At least three distinct strategies appear to allow such microorganisms to conserve energy in these oligotrophic environments: degradation of organic energy reserves, rhodopsin- and bacteriochlorophyll-dependent light harvesting, and oxidation of the atmospheric trace gases hydrogen and carbon monoxide. In turn, these principles are relevant for understanding the composition, functionality, and resilience of desert ecosystems, as well as predicting responses to the growing problem of desertification.
Phenotypic traits that convey information about individual identity or quality are important in animal social interactions, and the degree to which such traits are influenced by environmental variation can have profound effects on the reliability of these cues. Using inbred genetic lines of the decorated cricket, Gryllodes sigillatus, we manipulated diet quality to test how the cuticular hydrocarbon (CHC) profiles of males and females respond across two different nutritional rearing environments. There were significant differences between lines in the CHC profiles of females, but the effect of diet was not quite statistically significant. There was no significant genotype-by-environment interaction (GEI), suggesting that environmental effects on phenotypic variation in female CHCs are independent of genotype. There was, however, a significant effect of GEI for males, with changes in both signal quantity and content, suggesting that environmental effects on phenotypic expression of male CHCs are dependent on genotype. The differential response of male and female CHC expression to variation in the nutritional environment suggests that these chemical cues may be under sex-specific selection for signal reliability. Female CHCs show the characteristics of reliable cues of identity: high genetic variability, low condition dependence and a high degree of genetic determination. This supports earlier work showing that female CHCs are used in self-recognition to identify previous mates and facilitate polyandry. In contrast, male CHCs show the characteristics of reliable cues of quality: condition dependence and a relatively higher degree of environmental determination. This suggests that male CHCs are likely to function as cues of underlying quality during mate choice and/or male dominance interactions.
23Bacteria within aerated environments often exist within a variety of dormant forms. In 24 these states, bacteria endure adverse environmental conditions such as organic 25 carbon starvation by decreasing metabolic expenditure and using alternative energy 26 sources. In this study, we investigated the energy sources that facilitate the 27 persistence of the environmentally widespread but understudied bacterial phylum 28 Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class 29 Chloroflexia) extensively remodels its respiratory chain upon entry into stationary 30 phase due to organic carbon limitation. Whereas primary dehydrogenases associated 31 with heterotrophic respiration were downregulated, putative operons encoding 32 enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur 33 compound oxidation were significantly upregulated. Gas chromatography and 34 microsensor experiments were used to show that T. roseum aerobically respires H2 35 and CO at a range of environmentally relevant concentrations to sub-atmospheric 36 levels. Phylogenetic analysis suggests that the enzymes mediating atmospheric H2 37 and CO oxidation, namely group 1h [NiFe]-hydrogenases and type I carbon monoxide 38 dehydrogenases, are widely distributed in Chloroflexi genomes and have been 39 acquired on at least two occasions through separate horizontal gene transfer events. 40Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 41(class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence. This 42 study provides the first axenic culture evidence that atmospheric CO supports bacterial 43 persistence and reports the third phylum to be experimentally shown to mediate the 44 biogeochemically and ecologically important process of atmospheric H2 oxidation. This 45 adds to the growing body of evidence that atmospheric trace gases serve as 46 dependable energy sources for the survival of dormant microorganisms. 47 48 49 Bacteria from the phylum Chloroflexi are widespread and abundant in free-living 50 microbial communities [1-4]. One reason for their success is their metabolic diversity; 51 cultured strains from the phylum include heterotrophs, lithotrophs, and phototrophs 52 adapted to both oxic and anoxic environments [5]. Cultured representatives of the 53 phylum are classified into four classes by the genome taxonomy database [6], the 54 primarily aerobic Chloroflexia and Ktedonobacteria and the anaerobic Anaerolineae 55 and Dehalococcoidia [5]. Numerous studies have provided insight into the metabolic 56 strategies anaerobic classes within Chloroflexi use to adapt to oligotrophic niches [7, 57 8]. Surprisingly little, however, is known about how aerobic heterotrophic bacteria 58 within this phylum colonise oxic environments. Global surveys have reported that 59 Chloroflexi comprise 4.3% of soil bacteria [2] and 3.2% of marine bacteria [3]. However, 60 the most dominant lineages within these ecosystems (notably Ellin6524 and SAR202) 61 have proven...
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