Extracellular enzyme activity under subzero hypersaline conditions by model cold-adapted bacteria and Arctic sea-ice microbial communities

Showalter, G. M.; Deming, J. W.

doi:10.3354/ame01974

Cited by 5 publications

(5 citation statements)

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“…The seawater‐derived Colwellia populations (mainly C. hornerae and C. psychrerythraea ) have low‐temperature activities including chemotaxis, indicating active colonization and utilization of permafrost particles. Furthermore, extracellular enzymes from C. psychrerythraea degrade OC from melting sea‐ice (Showalter & Deming, 2021), and might be similarly active on permafrost OC. Presumed activities likely benefitted from specific genomic features, such as cold adaptation via polyunsaturated fatty acids synthesized by Colwellia , Psychrobacter , and Moritella (Bowman, 2017).…”

Section: Discussionmentioning

confidence: 99%

Microbial Communities Degrade Ancient Permafrost‐Derived Organic Matter in Arctic Seawater

Ruben,

Marchant,

Wietz

et al. 2024

JGR Biogeosciences

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The Arctic is experiencing rapid warming, which among other processes results in increasing erosion of coastal permafrost and the release of ancient organic carbon (OC) into the Arctic Ocean, which in turn might result in greenhouse gas emissions following its decomposition. Supply of terrigenous organic matter to the ocean affects near‐shore nutrient concentrations and the composition of microbial communities—highlighting the need to understand the fate of permafrost‐derived carbon in this fragile ecosystem. We incubated material from coastal Yedoma permafrost for 85 days in seawater collected during the Arctic Century expedition. During this experiment, 2.8 ± 1.4% of OC from coastal Yedoma was respired to CO2. Radiocarbon analysis revealed that 88 ± 15% of the released CO2 originated from ancient material (∼40,000 years), indicating that degradation of permafrost OC reintroduces old carbon into the short‐term carbon cycle. Hence, the permafrost climate feedback may be enhanced in the coming decades when coastal erosion accelerates. Additionally, 0.9 ± 0.3% of Yedoma OC was leached as dissolved OC. The observed net production of inorganic nitrogen during the incubation could potentially provide a negative feedback by stimulating primary production. Bacterial community analysis showed a succession of primary responders to biolabile substrates (e.g., Psychrobacter and Colwellia) followed by secondary consumers of less biolabile substrates (e.g., Maribacter and Pseudohongiella), plus a potential establishment of permafrost associated‐bacteria on particles. Overall, our data show that OC input from thawing permafrost stimulates bacterial dynamics, with likely implications for regional biogeochemical cycles and the Earth's climate.

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Section: Discussionmentioning

confidence: 99%

Microbial Communities Degrade Ancient Permafrost‐Derived Organic Matter in Arctic Seawater

Ruben,

Marchant,

Wietz

et al. 2024

JGR Biogeosciences

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“…As labile organics are consumed, more recalcitrant (sediment-adsorbed or permafrost-derived) forms of organic substrates may become important sources of nutrients for the community. Extracellular enzymes that degrade organic matter have been demonstrated to be active under cryopeg conditions ( Showalter and Deming, 2021 ), and the Marinobacter species characterized here are well equipped genetically to take advantage of the variety of substrates that can be produced by this general process. We suggest that Marinobacter spp.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Divergence of Marinobacter Strains in Cryopeg Brines as Revealed by Pangenomics

et al. 2022

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Marinobacter spp. are cosmopolitan in saline environments, displaying a diverse set of metabolisms that allow them to competitively occupy these environments, some of which can be extreme in both salinity and temperature. Here, we introduce a distinct cluster of Marinobacter genomes, composed of novel isolates and in silico assembled genomes obtained from subzero, hypersaline cryopeg brines, relic seawater-derived liquid habitats within permafrost sampled near Utqiaġvik, Alaska. Using these new genomes and 45 representative publicly available genomes of Marinobacter spp. from other settings, we assembled a pangenome to examine how the new extremophile members fit evolutionarily and ecologically, based on genetic potential and environmental source. This first genus-wide genomic analysis revealed that Marinobacter spp. in general encode metabolic pathways that are thermodynamically favored at low temperature, cover a broad range of organic compounds, and optimize protein usage, e.g., the Entner–Doudoroff pathway, the glyoxylate shunt, and amino acid metabolism. The new isolates contributed to a distinct clade of subzero brine-dwelling Marinobacter spp. that diverged genotypically and phylogenetically from all other Marinobacter members. The subzero brine clade displays genomic characteristics that may explain competitive adaptations to the extreme environments they inhabit, including more abundant membrane transport systems (e.g., for organic substrates, compatible solutes, and ions) and stress-induced transcriptional regulatory mechanisms (e.g., for cold and salt stress) than in the other Marinobacter clades. We also identified more abundant signatures of potential horizontal transfer of genes involved in transcription, the mobilome, and a variety of metabolite exchange systems, which led to considering the importance of this evolutionary mechanism in an extreme environment where adaptation via vertical evolution is physiologically rate limited. Assessing these new extremophile genomes in a pangenomic context has provided a unique view into the ecological and evolutionary history of the genus Marinobacter, particularly with regard to its remarkable diversity and its opportunism in extremely cold and saline environments.

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“…Based on a theorized incompatibility between the types of protein changes needed for hypersaline adaptation and psychrophilic adaptation [72], the evidence of cold adaptation in the form II Rubisco sequences may preclude a simultaneous adaptation to high salt conditions. Despite theoretical contentions, extracellular enzymes produced by psychrophilic bacteria have been shown to be active, in some cases preferentially active, under combined subzero and hypersaline conditions [73]. The environmental pressure to adapt to such extreme conditions would be limited for intracellular proteins, as they are not subjected to the ionic concentrations present for extracellular proteins, particularly in organisms that use compatible solutes, a common form of salt protection [72].…”

Section: Rubisco Adaptation To Extreme Environmentsmentioning

confidence: 99%

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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Extracellular enzyme activity under subzero hypersaline conditions by model cold-adapted bacteria and Arctic sea-ice microbial communities

Cited by 5 publications

References 0 publications

Microbial Communities Degrade Ancient Permafrost‐Derived Organic Matter in Arctic Seawater

Microbial Communities Degrade Ancient Permafrost‐Derived Organic Matter in Arctic Seawater

Evolutionary Divergence of Marinobacter Strains in Cryopeg Brines as Revealed by Pangenomics

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

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