scholarly journals Reconciling a Model of Core Metabolism with Growth Yield Predicts Biochemical Mechanisms and Efficiency for a Versatile Chemoautotroph

2019 ◽  
Author(s):  
Jesse McNichol ◽  
Stefan M. Sievert
Keyword(s):  
Comparative Genomics ◽  
Energy Conservation ◽  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Conceptual Modeling ◽  
Growth Yield ◽  
Sulfur Oxidation ◽  
Growth Efficiency ◽  
Biochemical Mechanisms ◽  
Core Metabolism

AbstractObligately chemoautotrophic Campylobacteria dominate productivity in dark, sulfidic, and oxygen-depleted environments. However, biochemical mechanisms underlying their growth remain poorly known, limiting understanding of their physiology, ecology, and biogeochemical impact. In this study, we used comparative genomics, conceptual modeling of core metabolism, and chemostat growth yields to derive a model of energy conservation consistent with experimental data for the versatile chemoautotroph Sulfurimonas denitrificans. Our model rests on three core mechanisms: Firstly, to allow electrogenic sulfur-based denitrification, we predict that the campylobacterial-type sulfur oxidation enzyme complex must donate electrons to the membrane quinone pool, possibly via a sulfide:quinone oxidoreductase. Secondly, to account for the unexpectedly low growth efficiency of aerobic sulfur oxidation compared to denitrification, we posit the high-affinity campylobacterial-type cbb3 cytochrome c oxidase has a relatively low H+/e− of 1, likely due to a lack of proton pumping under physiological conditions. Thirdly, we hypothesize that reductant for carbon fixation by the reverse tricarboxylic acid cycle is produced by a non-canonical complex I that reduces both ferredoxin and NAD(P)H. This complex is conserved among related Campylobacteria and may have allowed for the radiation of organisms like S. denitrificans into sulfur-rich environments that became available after the great oxidation event. Our theoretical model has two major implications. Firstly, it sets the stage for future experimental work by providing testable hypotheses about the physiology, biochemistry, and evolution of chemoautotrophic Campylobacteria. Secondly, it provides constraints on the carbon fixation potential of chemoautotrophic Campylobacteria in sulfidic environments worldwide by predicting theoretical ranges of chemosynthetic growth efficiency.SignificanceChemoautotrophic Campylobacteria are abundant in many low-oxygen, high-sulfide environments where they contribute significantly to dark carbon fixation. Although the overall redox reactions they catalyze are known, the specific biochemical mechanisms that support their growth are mostly unknown. Our study combines conceptual modeling of core metabolic pathways, comparative genomics, and measurements of physiological growth yield in a chemostat to infer the most likely mechanisms of chemoautotrophic energy conservation in the model organism Sulfurimonas denitrificans. The hypotheses proposed herein are novel, experimentally falsifiable, and will guide future biochemical, physiological, and environmental modelling studies. Ultimately, investigating the core mechanisms of energy conservation will help us better understand the evolution and physiological diversification of chemoautotrophic Campylobacteria and their role in modern ecosystems.

scholarly journals Comparative Genome Analysis of the Genus Thiothrix Involving Three Novel Species, Thiothrix subterranea sp. nov. Ku-5, Thiothrix litoralis sp. nov. AS and “Candidatus Thiothrix anitrata” sp. nov. A52, Revealed the Conservation of the Pathways of Dissimilatory Sulfur Metabolism and Variations in the Genetic Inventory for Nitrogen Metabolism and Autotrophic Carbon Fixation

2021 ◽  
Vol 12 ◽  
Author(s):  
Nikolai V. Ravin ◽  
Tatyana S. Rudenko ◽  
Dmitry D. Smolyakov ◽  
Alexey V. Beletsky ◽  
Andrey L. Rakitin ◽  
...  
Keyword(s):  
Core Genome ◽  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Sulfur Metabolism ◽  
Sulfide Oxidation ◽  
Calvin Cycle ◽  
Sulfur Oxidation ◽  
Rrna Gene ◽  
Reduced Sulfur Compounds ◽  
Hybridization Data

Two strains of filamentous, colorless sulfur bacteria were isolated from bacterial fouling in the outflow of hydrogen sulfide-containing waters from a coal mine (Thiothrix sp. Ku-5) and on the seashore of the White Sea (Thiothrix sp. AS). Metagenome-assembled genome (MAG) A52 was obtained from a sulfidic spring in the Volgograd region, Russia. Phylogenetic analysis based on the 16S rRNA gene sequences showed that all genomes represented the genus Thiothrix. Based on their average nucleotide identity and digital DNA-DNA hybridization data these new isolates and the MAG represent three species within the genus Thiothrix with the proposed names Thiothrix subterranea sp. nov. Ku-5T, Thiothrix litoralis sp. nov. AST, and “Candidatus Thiothrix anitrata” sp. nov. A52. The complete genome sequences of Thiothrix fructosivorans QT and Thiothrix unzii A1T were determined. Complete genomes of seven Thiothrix isolates, as well as two MAGs, were used for pangenome analysis. The Thiothrix core genome consisted of 1,355 genes, including ones for the glycolysis, the tricarboxylic acid cycle, the aerobic respiratory chain, and the Calvin cycle of carbon fixation. Genes for dissimilatory oxidation of reduced sulfur compounds, namely the branched SOX system (SoxAXBYZ), direct (soeABC) and indirect (aprAB, sat) pathways of sulfite oxidation, sulfur oxidation complex Dsr (dsrABEFHCEMKLJONR), sulfide oxidation systems SQR (sqrA, sqrF), and FCSD (fccAB) were found in the core genome. Genomes differ in the set of genes for dissimilatory reduction of nitrogen compounds, nitrogen fixation, and the presence of various types of RuBisCO.

scholarly journals Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria

Microbiome ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Marie-Anne Cambon-Bonavita ◽  
Johanne Aubé ◽  
Valérie Cueff-Gauchard ◽  
Julie Reveillaud
Keyword(s):  
Hydrothermal Vents ◽  
Carbon Fixation ◽  
Iron Sulfide ◽  
Hydrogen Oxidation ◽  
Niche Partitioning ◽  
Sulfur Oxidation ◽  
Single Copy ◽  
Trophic Levels ◽  
Rimicaris Exoculata ◽  
Close Relatives

Abstract Background Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata, which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria, Desulfobulbia (formerly Deltaproteobacteria), Alphaproteobacteria, Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris–microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria, Desulfobulbia, Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.

Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment

2010 ◽  
Vol 13 (3) ◽  
pp. 758-774 ◽  
Author(s):  
Sabine Lenk ◽  
Julia Arnds ◽  
Katrice Zerjatke ◽  
Niculina Musat ◽  
Rudolf Amann ◽  
...  
Keyword(s):  
Carbon Fixation ◽  
Sulfur Oxidation ◽  
Intertidal Sediment

scholarly journals Geobacter sulfurreducens inner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration

2021 ◽  
Author(s):  
Komal Joshi ◽  
Chi Ho Chan ◽  
Daniel R. Bond
Keyword(s):  
Electron Transfer ◽  
Redox Potential ◽  
Growth Yield ◽  
Growth Efficiency ◽  
Geobacter Sulfurreducens ◽  
Redox Potentials ◽  
Hydrogen Electrode ◽  
Highly Expressed Genes ◽  
Reducing Bacteria ◽  
Transfer Chain

AbstractGeobacter sulfurreducens utilizes extracellular electron acceptors such as Mn(IV), Fe(III), syntrophic partners, and electrodes that vary from +0.4 to −0.3 V vs. Standard Hydrogen Electrode (SHE), representing a potential energy span that should require a highly branched electron transfer chain. Here we describe CbcBA, a bc-type cytochrome essential near the thermodynamic limit of respiration when acetate is the electron donor. Mutants lacking cbcBA ceased Fe(III) reduction at −0.21 V vs. SHE, could not transfer electrons to electrodes between −0.21 and −0.28 V, and could not reduce the final 10% – 35% of Fe(III) minerals. As redox potential decreased during Fe(III) reduction, cbcBA was induced with the aid of the regulator BccR to become one of the most highly expressed genes in G. sulfurreducens. Growth yield (CFU/mM Fe(II)) was 112% of WT in ΔcbcBA, and deletion of cbcL (a different bc-cytochrome essential near −0.15 V) in ΔcbcBA increased yield to 220%. Together with ImcH, which is required at high redox potentials, CbcBA represents a third cytoplasmic membrane oxidoreductase in G. sulfurreducens. This expanding list shows how these important metal-reducing bacteria may constantly sense redox potential to adjust growth efficiency in changing environments.

scholarly journals Unraveling Fe(II)-oxidizing mechanisms in a facultative Fe(II) oxidizer Sideroxydans lithotrophicus ES-1 via culturing, transcriptomics, and RT-qPCR

2021 ◽  
Author(s):  
Nanqing Zhou ◽  
Jessica L. Keffer ◽  
Shawn W. Polson ◽  
Clara S Chan
Keyword(s):  
Gene Expression ◽  
Carbon Fixation ◽  
Expression Profiles ◽  
Gene Expression Profiles ◽  
Sulfur Oxidation ◽  
Complex Iii ◽  
Initial Growth ◽  
Gene Expression Response ◽  
Oxidase Gene ◽  
Thiosulfate Oxidation

Sideroxydans lithotrophicus ES-1 grows autotrophically either by Fe(II) oxidation or thiosulfate oxidation, in contrast to most other neutrophilic Fe(II)-oxidizing bacteria (FeOB) isolates. This provides a unique opportunity to explore the physiology of a facultative FeOB and constrain the genes specific to Fe(II) oxidation. We compared the growth of S. lithotrophicus ES-1 on Fe(II), thiosulfate, and both substrates together. While initial growth rates were similar, thiosulfate-grown cultures had higher yield with or without Fe(II) present, which may give ES-1 an advantage over obligate FeOB. To investigate the Fe(II) and S oxidation pathways, we conducted transcriptomics experiments, validated with RT-qPCR. We explored the long-term gene expression response at different growth phases (over days-week) and expression changes during a short-term switch from thiosulfate to Fe(II) (90 min). The dsr and sox sulfur oxidation genes were upregulated in thiosulfate cultures. The Fe(II) oxidase gene cyc2 was among the top expressed genes during both Fe(II) and thiosulfate oxidation, and addition of Fe(II) to thiosulfate-grown cells caused an increase in cyc2 expression. These results support the role of Cyc2 as the Fe(II) oxidase and suggest that ES-1 maintains readiness to oxidize Fe(II) even in the absence of Fe(II). We used gene expression profiles to further constrain the ES-1 Fe(II) oxidation pathway. Notably, among the most highly upregulated genes during Fe(II) oxidation were genes for alternative complex III, reverse electron transport and carbon fixation. This implies a direct connection between Fe(II) oxidation and carbon fixation, suggesting that CO2 is an important electron sink for Fe(II) oxidation.

scholarly journals Kinetics of the ancestral carbon metabolism pathways in deep-branching bacteria and archaea

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Tomonari Sumi ◽  
Kouji Harada
Keyword(s):  
Carbon Metabolism ◽  
Carbon Fixation ◽  
Citrate Synthase ◽  
Tricarboxylic Acid Cycle ◽  
Necessary Condition ◽  
Last Universal Common Ancestor ◽  
Universal Common Ancestor ◽  
Biomass Components ◽  
Kinetics Of ◽  
Reductive Tricarboxylic Acid Cycle

AbstractThe origin of life is believed to be chemoautotrophic, deriving all biomass components from carbon dioxide, and all energy from inorganic redox couples in the environment. The reductive tricarboxylic acid cycle (rTCA) and the Wood–Ljungdahl pathway (WL) have been recognized as the most ancient carbon fixation pathways. The rTCA of the chemolithotrophic Thermosulfidibacter takaii, which was recently demonstrated to take place via an unexpected reverse reaction of citrate synthase, was reproduced using a kinetic network model, and a competition between reductive and oxidative fluxes on rTCA due to an acetyl coenzyme A (ACOA) influx upon acetate uptake was revealed. Avoiding ACOA direct influx into rTCA from WL is, therefore, raised as a kinetically necessary condition to maintain a complete rTCA. This hypothesis was confirmed for deep-branching bacteria and archaea, and explains the kinetic factors governing elementary processes in carbon metabolism evolution from the last universal common ancestor.

MdUGT88F1-mediated phloridzin biosynthesis coordinates carbon and nitrogen accumulation in apple

2021 ◽  
Author(s):  
Kun Zhou ◽  
Lingyu Hu ◽  
Hong Yue ◽  
Zhijun Zhang ◽  
Jingyun Zhang ◽  
...  
Keyword(s):  
Carbon Fixation ◽  
Chloroplast Development ◽  
Tricarboxylic Acid Cycle ◽  
Ammonium Assimilation ◽  
Light Sensitivity ◽  
Sugar Accumulation ◽  
Nitrogen Accumulation ◽  
High Accumulation ◽  
Carbon And Nitrogen

Abstract The high accumulation of phloridzin makes apple (Malus domestica) unique in the plant kingdom, which suggests a vital role of its biosynthesis in the physiological processes of apple. In our previous study, silencing MdUGT88F1 (a key UDP-glucose: phloretin 2'-O-glucosyltransferase gene) revealed the importance of phloridzin biosynthesis in apple development and Valsa canker resistance. Here, results from MdUGT88F1-silencing lines showed that phloridzin biosynthesis was indispensable for normal chloroplast development and photosynthetic carbon fixation by maintaining MdGLK1/2 expression. Interestingly, the increased phloridzin biosynthesis didn’t affect plant (or chloroplast) development but reduced nitrogen accumulation, leading to chlorophyll deficiency, light sensitivity, and sugar accumulation in MdUGT88F1-overexpressing apple lines during their growth and development. Further analysis revealed that MdUGT88F1-mediated phloridzin biosynthesis negatively regulated cytosolic glutamine synthetase1-asparagine synthetase-asparaginase (GS1-AS-ASPG) pathway of ammonium assimilation and limited chlorophyll synthesis in the shoots of apple. The interference of phloridzin biosynthesis in the GS1-AS-ASPG pathway was also assumed to be associated with its limitation of the carbon skeletons of ammonium assimilation through metabolic competition with the tricarboxylic acid cycle. Taken together, our findings shed light on the role of MdUGT88F1-mediated phloridzin biosynthesis in the coordination between carbon and nitrogen accumulation in apple trees.

scholarly journals Abiotic and biotic processes that drive carboxylation and decarboxylation reactions

2020 ◽  
Vol 105 (5) ◽  
pp. 609-615
Author(s):  
Cody S. Sheik ◽  
H. James Cleaves ◽  
Kristin Johnson-Finn ◽  
Donato Giovannelli ◽  
Thomas L. Kieft ◽  
...  
Keyword(s):  
Metabolic Pathways ◽  
Subduction Zones ◽  
Carbon Fixation ◽  
Prebiotic Chemistry ◽  
Tricarboxylic Acid Cycle ◽  
Tricarboxylic Acid ◽  
Short Term ◽  
Planetary Evolution ◽  
Broad Overview

Abstract Carboxylation and decarboxylation are two fundamental classes of reactions that impact the cycling of carbon in and on Earth’s crust. These reactions play important roles in both long-term (primarily abiotic) and short-term (primarily biotic) carbon cycling. Long-term cycling is important in the subsurface and at subduction zones where organic carbon is decomposed and outgassed or recycled back to the mantle. Short-term reactions are driven by biology and have the ability to rapidly convert CO2 to biomass and vice versa. For instance, carboxylation is a critical reaction in primary production and metabolic pathways like photosynthesis in which sunlight provides energy to drive carbon fixation, whereas decarboxylation is a critical reaction in metabolic pathways like respiration and the tricarboxylic acid cycle. Early life and prebiotic chemistry on Earth likely relied heavily upon the abiotic synthesis of carboxylic acids. Over time, life has diversified (de)carboxylation reactions and incorporated them into many facets of cellular metabolism. Here we present a broad overview of the importance of carboxylation and decarboxylation reactions from both abiotic and biotic perspectives to highlight the importance of these reactions and compounds to planetary evolution.

scholarly journals Genomic and Metabolic Insights into Two Novel Thiothrix Species from Enhanced Biological Phosphorus Removal Systems

2020 ◽  
Vol 8 (12) ◽  
pp. 2030
Author(s):  
Andrey V. Mardanov ◽  
Eugeny V. Gruzdev ◽  
Dmitry D. Smolyakov ◽  
Tatyana S. Rudenko ◽  
Alexey V. Beletsky ◽  
...  
Keyword(s):  
Phosphorus Removal ◽  
Tricarboxylic Acid Cycle ◽  
Sulfide Oxidation ◽  
Sulfur Oxidation ◽  
Co2 Assimilation ◽  
Amino Acid Identity ◽  
Rrna Gene ◽  
Enhanced Biological Phosphorus Removal ◽  
Biological Phosphorus Removal ◽  
Biological Phosphorus

Two metagenome-assembled genomes (MAGs), obtained from laboratory-scale enhanced biological phosphorus removal bioreactors, were analyzed. The values of 16S rRNA gene sequence identity, average nucleotide identity, and average amino acid identity indicated that these genomes, designated as RT and SSD2, represented two novel species within the genus Thiothrix, ‘Candidatus Thiothrix moscowensis’ and ‘Candidatus Thiothrix singaporensis’. A complete set of genes for the tricarboxylic acid cycle and electron transport chain indicates a respiratory type of metabolism. A notable feature of RT and SSD2, as well as other Thiothrix species, is the presence of a flavin adenine dinucleotide (FAD)-dependent malate:quinone oxidoreductase instead of nicotinamide adenine dinucleotide (NAD)-dependent malate dehydrogenase. Both MAGs contained genes for CO2 assimilation through the Calvin–Benson–Bassam cycle; sulfide oxidation (sqr, fccAB), sulfur oxidation (rDsr complex), direct (soeABC) and indirect (aprBA, sat) sulfite oxidation, and the branched Sox pathway (SoxAXBYZ) of thiosulfate oxidation to sulfur and sulfate. All these features indicate a chemoorganoheterotrophic, chemolithoautotrophic, and chemolithoheterotrophic lifestyle. Both MAGs comprise genes for nitrate reductase and NO-reductase, while SSD2 also contains genes for nitrite reductase. The presence of polyphosphate kinase and exopolyphosphatase suggests that RT and SSD2 could accumulate and degrade polyhosphates during the oxic-anoxic growth cycle in the bioreactors, such as typical phosphate-accumulating microorganisms.

scholarly journals Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer

mSystems ◽  
2020 ◽  
Vol 5 (2) ◽  
Author(s):  
Lauren M. Seyler ◽  
William J. Brazelton ◽  
Craig McLean ◽  
Lindsay I. Putman ◽  
Alex Hyer ◽  
...  
Keyword(s):  
Microbial Communities ◽  
Carbon Fixation ◽  
Dissolved Inorganic Carbon ◽  
Sequence Data ◽  
Tricarboxylic Acid Cycle ◽  
Carbon Sources ◽  
Mass Spectrometry Data ◽  
Physiological Adaptation ◽  
Coast Range ◽  
Coast Range Ophiolite

ABSTRACT Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. Such reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry mediated by microbial populations that inhabit these environments is understudied and complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of 12 wells drilled into the ultramafic and serpentinite mélange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we found evidence for several carbon fixation and assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl coenzyme A (acetyl-CoA) pathway, and methylotrophy, in the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggest that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable. IMPORTANCE This study describes the potential metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor and at continental margins, where ancient seafloor has accreted onto the continents. Because of the difficulty in delineating abiotic and biotic processes in these environments, major questions remain related to microbial contributions to the carbon cycle and physiological adaptation to serpentinite habitats. This research explores multiple mechanisms of carbon fixation and assimilation in serpentinite-hosted microbial communities.

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