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LaRowe, D. E.

Publications and source records attributed to LaRowe, D. E..

7 recordsLinked to original sources

Compositional Heterogeneity Structures Microbial Microhabitats across Distinct Mineral Substrates

Microbial communities living on and in rocks operate at the microscale, where interactions with minerals fundamentally shape community structure and function. Yet the relationship between micron scale mineralogical configurations and microbial distributions remains poorly understood. We tested the hypothesis that microbial biomass spatially correlates with areas of heightened mineralogical heterogeneity by applying Raman microspectroscopy to rock samples from three geologically distinct substrates: authigenic carbonates from a marine methane seep, volcanic basalt from Iceland, and polymetallic nodules from the abyssal seafloor. Using spectral decomposition and multiple complementary metrics of compositional heterogeneity, we evaluated intra-pixel and inter-pixel heterogeneity patterns in relation to biomass distribution. Our analyses reveal three patterns across all sample types. 1) When spectra are deconstructed into their constituent components, biomass zones are disproportionately dominated by the biomass spectral component compared with primary mineral components in zones of different minerals. 2) Biomass spectra have more homogeneous compositional profiles than mineral spectra. 3) Biomass is surrounded by more heterogeneous microhabitats than mineral pixels. These findings demonstrate that biomass exerts a distinctive and consistent influence on Raman spectral signatures, both within and between pixels, in ways that mineral components do not. Our results establish generalizable principles linking microscale mineralogical properties to microbial biogeography; these properties could be used as a potential biosignature and may provide a standardized workflow applicable to diverse rock systems and astrobiological exploration strategies.

microbiology↗

Acetogenic methane-carbon monoxide comproportionation: an exergonic but unobserved microbial metabolism

Microbial metabolism relies on redox reactions that exploit chemical disequilibria. While aerobic carbon oxidation, carbon fixation, and fermentation are well studied, the broader space of anaerobic carbon redox reactions remains underexplored. In this study, carbon comproportionation, or reverse fermentation, reactions are identified as a previously unrecognized and potentially favorable class of microbial carbon redox transformations. Particular attention is given to the reaction between methane (CH4) and carbon monoxide (CO) to form acetate, a reaction that has not previously been evaluated despite the widespread occurrence of CH4 and CO in anoxic systems. Gibbs energies ({Delta}Gr) for this reaction were calculated across broad ranges of temperature, pH, and dissolved CH4 and CO concentrations using measured physicochemical data from a wide variety of environmental systems. We show that acetogenic CH4-CO comproportionation is exergonic in all environments where both substrates were detected. The most favorable energetic conditions occur at high pH, low temperature, and high reactant concentrations, consistent with cool serpentinizing systems. In several settings, the calculated Gibbs energy yields and energy densities overlap or exceed known anaerobic metabolisms involving CH4, CO, and acetate. These results demonstrate that acetogenic CH4-CO comproportionation can support microbial energy conservation in a variety of settings. To determine if this metabolism could have operated on early Earth or Mars, modeled fluid compositions show that this reaction is also exergonic under plausible physicochemical regimes. This work broadens the suite of possible microbial energy metabolisms and provides testable criteria for evaluating carbon-based catabolic reactions on Earth and on other planetary bodies. Plain Language SummaryMicroorganisms obtain energy by catalyzing chemical reactions in their environment. The energy available from a reaction can be quantified using Gibbs energies of reaction ({Delta}Gr). When {Delta}Gr < 0, energy is released that microorganisms can use to build biomass and carry out other activities. In this study, we predicted a new energy-yielding reaction that could potentially support microbial life. In this reaction, methane (CH4) is oxidized using carbon monoxide (CO) to produce acetate. Using thermodynamic calculations and measured geochemical data from natural environments, we show that this reaction can release usable energy under a wide range of conditions, including continental serpentinizing systems, the deep continental and marine subsurface, and geothermal springs. We also predict that this reaction could support life under plausible early Earth conditions and in modeled Martian fluids. Together, these observations identify the reaction of CH4 and CO to form acetate as a potentially viable microbial energy source in anoxic environments on Earth and other planetary bodies.

microbiology↗

Isolation of a putative sulfur comproportionating microorganism

Sulfur comproportionation is a heretofore undiscovered microbial catabolism that was predicted based on thermodynamic calculations. Here, we report the isolation of an Acidithiobacillus thiooxidans strain from extremely low pH snottite biofilms in the karst at Frasassi, Italy. The strain grew to cell densities of >107 cells mL-1 in autotrophic sulfur comproportionation medium. Whole genome sequencing of the isolate revealed the presence of numerous genes involved in sulfur transformations that could be linked in a sulfur comproportionation pathway. We describe an experimental framework, including measurements of sulfate, sulfide, and S0 concentrations, electron microscopy, and stable and radioisotope incubations coupled with NanoSIMS, scintillation counting and isotope ratio mass spectrometry, for future searches of sulfur comproportionators. SignificanceThe prediction of and search for novel microbial catabolic reactions can be streamlined by using thermodynamics to identify energy-yielding redox reactions that may be catalyzed by microorganisms. This strategy has been used to successfully predict several previously overlooked microbial catabolic reactions, including anaerobic ammonia oxidation (anammox), anaerobic oxidation of methane (AOM), and complete ammonia oxidation (comammox). Sulfur comproportionation, or the coupled reduction of sulfate and oxidation of sulfide to form elemental sulfur, was predicted by thermodynamic calculations to exist as a microbial catabolism in low pH, low-temperature environments. In this study, we describe the isolation of the first putative sulfur comproportionating microorganism and provide a detailed experimental approach that can be applied to future investigations of this novel link in the biogeochemical sulfur cycle.

microbiology↗

Sulfur disproportionating microbial communities in a dynamic, microoxic-sulfidic karst system

Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen-rich meteoric water, creating Proterozoic-like conditions and supporting a prolific ecosystem driven by sulfur-based chemolithoautotrophy. To better understand the cycling of S0 in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide-oxidizing mats dominated by Beggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related to Sulfurovum, Halothiobacillus, Thiofaba, Thiovirga, Thiobacillus, and Desulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated with Bacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae. Desulfocapsa and Sulfurovum populations accounted for 12-26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S0 disproportionation in pure culture. Gibbs energy ({Delta}Gr) calculations revealed that S0 disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat-sediment interface showed that Beggiatoa mats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S0 generated by microbial sulfide oxidation in this oxygen-limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur- rich environments.

microbiology↗

Quantifying the bioavailable energy in an ancient hydrothermal vent on Mars and a modern Earth-based analogue.

Putative alkaline hydrothermal systems on Noachian Mars were potentially habitable environments for microorganisms. However, the types of reactions that could have fueled microbial life in such systems and the amount of energy available from them have not been quantitatively constrained. In this study, we use thermodynamic modeling to calculate which catabolic reactions could have supported ancient life in a saponite-precipitating hydrothermal vent system in the Eridania basin on Mars. To further evaluate what this could mean for microbial life, we evaluated the energy potential of an analogue site in Iceland, the Strytan Hydrothermal Field (SHF). Results show that out of the 85 relevant redox reactions that were considered, the highest energy-yielding reactions in the Eridania hydrothermal system were dominated by methane formation. By contrast, Gibbs energy calculations carried out for Strytan indicate that the most energetically favorable reactions are CO2 and O2 reduction coupled to H2 oxidation. In particular, our calculations indicate that an ancient hydrothermal system within the Eridania basin could have been a habitable environment for methanogens using NH4+ as an electron acceptor. Differences in Gibbs energies between the two systems were largely determined by oxygen - its presence on Earth and absence on Mars. However, Strytan can serve as a useful analogue for Eridania when studying methane producing reactions that do not involve O2.

microbiology↗

Ecophysiology of the cosmopolitan OM252 bacterioplankton (Gammaproteobacteria)

Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria. Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (Candidatus Halomarinus), sister to Litoricola, comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors, with subclade I genomes encoding the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance but a mesophilic temperature range for growth, with a maximum of 0.36 doublings/hr at 35{degrees}C. Cells were curved rod/spirillum-shaped, ~1.5 x 0.2 m. Growth on thiosulfate as the sole electron donor under autotrophic conditions was roughly one third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some Ca. Halomarinus organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. ImportanceMarine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria, has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic datasets, we examined the diversity within the OM252 clade, the distribution of these taxa in the worlds oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point towards the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly "heterotrophic" taxa.

microbiology↗

Another chemolithotrophic metabolism missing in nature--sulfur comproportionation

Chemotrophic microorganisms gain energy for cellular functions by catalyzing oxidation-reduction (redox) reactions that are out of equilibrium. Calculations of the Gibbs energy ({Delta}Gr) can identify whether a reaction is thermodynamically favorable, and the accompanying energy yield at the temperature, pressure, and chemical composition in the system of interest. Based on carefully calculated values of {Delta}Gr, we predict a novel microbial metabolism--sulfur comproportionation (3H2S + SO42- + 2H+ = 4S0 + 4H2O). We show that at elevated concentrations of sulfide and sulfate in acidic environments over a broad temperature range, this putative metabolism can be exergonic ({Delta}Gr<0), yielding [~]30-50 kJ/mol. We suggest that this may be sufficient energy to support a chemolithotrophic metabolism currently missing in nature. Other versions of this metabolism, to thiosulfate (H2S + SO42- = S2O32- + H2O) and to sulfite (H2S + 3SO42- = 4SO32- + 2H+), are only moderately exergonic or endergonic even at ideal geochemical conditions. Natural and impacted environments, including sulfidic karst systems, shallow-sea hydrothermal vents, sites of acid mine drainage, and acid-sulfate crater lakes, may be ideal hunting grounds for finding microbial sulfur comproportionators.

microbiology↗