Metagenomics untangles metabolic adaptations of Antarctic endolithic bacteria at the fringe of habitability

Coleine, Claudia; Albanese, Davide; Ray, Angelique E.; Delgado-Baquerizo, Manuel; Stajich, Jason E.; Williams, Timothy J.; Larsen, Stefano; Tringe, Susannah; Pennacchio, Christa; Ferrari, Belinda C.; Donati, Claudio; Selbmann, Laura

doi:10.1101/2023.07.30.551190

Cited by 2 publications

References 23 publications

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Prevalence of the Calvin-Benson-Bassham cycle in chemolithoautotrophic psychrophiles and the potential for cold-adapted Rubisco

Harrison,

Rapp,

Jaffe

et al. 2024

Preprint

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The act of fixing inorganic carbon into the biosphere is largely facilitated by one enzyme, Rubisco. Beyond well-studied plants and cyanobacteria, many bacteria use Rubisco for chemolithoautotrophy in extreme environments on Earth. Here, we characterized the diversity of chemolithoautotrophic Rubiscos in subzero environments. First, we surveyed subzero environments and found that the Calvin-Benson-Bassham cycle was the most prevalent chemolithoautotrophic pathway. Second, we uncovered potential for chemolithoautotrophy in metagenomes from two distinct subzero, hypersaline Arctic environments: 40-kyr relic marine brines encased within permafrost (cryopeg brines) and first-year sea ice. Again, the Calvin-Benson-Bassham cycle was the dominant chemolithoautotrophic pathway in both environments, though with different Rubisco forms. From cryopeg brine, we reconstructed four metagenome-assembled genomes with the potential for chemolithoautotrophy, of which the sulfur-oxidizing genusThiomicrorhabduswas most abundant. A broader survey ofThiomicrorhabdusgenomes from diverse environments identified a core complement of three Rubisco forms (II, IAc, IAq) with distinct patterns of gain and loss. We developed a model framework and compared these different Rubisco forms across [CO2], [O2], and temperature. We found that form II outcompetes form I at low O2, but cold temperatures minimize this advantage. However, further inspection of form II from cold environments uncovered signals of thermal adaptation of key amino acids which resulted in a more exposed active site. These modifications suggest that these form II Rubisco proteins may have unique kinetics or thermal stability. This work can help address the limits of autotrophic functionality in extreme environments on Earth and other planetary bodies.ImportanceAutotrophy, or the fixation of inorganic carbon to biomass, is a key factor in life’s ability to thrive on Earth. Research on autotrophy has focused on plants and algae, but many bacteria are also autotrophic and can survive and thrive under more extreme conditions. These bacteria are a window to past autotrophy on Earth, as well as potential autotrophy in extreme environments elsewhere in the Universe. Our study focused on dark, cold, saline environments, which are likely to be found on Enceladus and Europa, as well as in the Martian subsurface. We found compelling evidence of cold adaptation in a key autotrophic enzyme, Rubisco, which could expand the known boundaries of autotrophy in rapidly disappearing icy environments on Earth. We also present a novel model framework that can be used to probe the limits of autotrophy not only on Earth but also on key astrobiological targets like Enceladus and Europa.

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Prevalence of the Calvin-Benson-Bassham cycle in chemolithoautotrophic psychrophiles and the potential for cold-adapted Rubisco

Harrison,

Rapp,

Jaffe

et al. 2024

Preprint

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Novel endolithic bacteria of phylum Chloroflexota reveal a myriad of potential survival strategies in the Antarctic desert

Williams,

Allen,

Ray

et al. 2024

Appl Environ Microbiol

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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 H 2 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. IMPORTANCE The 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.

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Metagenomics untangles metabolic adaptations of Antarctic endolithic bacteria at the fringe of habitability

Cited by 2 publications

References 23 publications

Prevalence of the Calvin-Benson-Bassham cycle in chemolithoautotrophic psychrophiles and the potential for cold-adapted Rubisco

Prevalence of the Calvin-Benson-Bassham cycle in chemolithoautotrophic psychrophiles and the potential for cold-adapted Rubisco

Novel endolithic bacteria of phylum Chloroflexota reveal a myriad of potential survival strategies in the Antarctic desert

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