Metabolic overlap in environmentally diverse microbial communities

Contains fulltext : 209073.pdf (preprint version ) (Open Access)The majority of microbial communities consist of hundreds to thousands of species, creating a massive network of organisms competing for available resources within an ecosystem. In natural microbial communities it appears that many microbial species have highly redundant metabolisms and seemingly are capable of utilizing the same substrates. This is paradoxical, as theory indicates that species requiring a common resource should outcompete one another. To better understand why microbial species can co-exist, we developed Metabolic Overlap (MO) as a new metric to survey the functional redundancy of microbial communities at the genome scale across a wide variety of ecosystems. Using metagenome-assembled genomes, we surveyed over 1200 studies across ten ecosystem types. We found the highest MO in extreme (i.e., low pH/high temperature) and aquatic environments, while the lowest MO was observed in communities associated with animal hosts, or the built/engineered environment. In addition, different metabolism subcategories were explored for their degree of metabolic overlap. For instance, overlap in nitrogen metabolism was among the lowest in Animal and Engineered ecosystems, while the most was in species from the Built environment. Together, we present a metric that utilizes whole genome information to explore overlapping niches of microbes. This provides a detailed picture of potential metabolic competition and cooperation between species present in an ecosystem, indicates the main substrate types sustaining the community and serves as a valuable tool to generate hypotheses for future research.01 januari 201

A unique bacteriohopanetetrol stereoisomer of marine anammox

Anaerobic ammonium oxidation (anammox) is a major process of bioavailable nitrogen removal from marine systems. Previously, a bacteriohopanetetrol (BHT) isomer, with unknown stereochemistry, eluting later than BHT using high performance liquid chromatography (HPLC), was detected in ‘Ca. Scalindua profunda’ and proposed as a biomarker for anammox in marine paleo-environments. However, the utility of this BHT isomer as an anammox biomarker is hindered by the fact that four other, non-anammox bacteria are also known to produce a late-eluting BHT stereoisomer. The stereochemistry in Acetobacter pasteurianus, Komagataeibacter xylinus and Frankia sp. was known to be 17β, 21β(H), 22R, 32R, 33R, 34R (BHT-34R). The stereochemistry of the late-eluting BHT in Methylocella palustris was unknown. To determine if marine anammox bacteria produce a unique BHT isomer, we studied the BHT distributions and stereochemistry of known BHT isomer producers and of previously unscreened marine (‘Ca. Scalindua brodeae’) and freshwater (‘Ca. Brocadia sp.’) anammox bacteria using HPLC and gas chromatographic (GC) analysis of acetylated BHTs and ultra high performance liquid chromatography (UHPLC)-high resolution mass spectrometry (HRMS) analysis of non-acetylated BHTs. The 34R stereochemistry was confirmed for the BHT isomers in Ca. Brocadia sp. and Methylocella palustris. However, ‘Ca. Scalindua sp.’ synthesise a stereochemically distinct BHT isomer, with still unconfirmed stereochemistry (BHT-x). Only GC analysis of acetylated BHT and UHPLC analysis of non-acetylated BHT distinguished between late-eluting BHT isomers. Acetylated BHT-x and BHT-34R co-elute by HPLC. As BHT-x is currently only known to be produced by ‘Ca. Scalindua spp.’, it may be a biomarker for marine anammox

The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H₂ with a high-affinity, membrane-associated [NiFe] hydrogenase

The trace amounts (0.53 ppmv) of atmospheric hydrogen gas (H2) can be utilized by microorganisms to persist during dormancy. This process is catalyzed by certain Actinobacteria, Acidobacteria, and Chloroflexi, and is estimated to convert 75 × 1012 g H2 annually, which is half of the total atmospheric H2. This rapid atmospheric H2 turnover is hypothesized to be catalyzed by high-affinity [NiFe] hydrogenases. However, apparent high-affinity H2 oxidation has only been shown in whole cells, rather than for the purified enzyme. Here, we show that the membrane-associated hydrogenase from the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV possesses a high apparent affinity (Km(app) = 140 nM) for H2 and that methanotrophs can oxidize subatmospheric H2. Our findings add to the evidence that the group 1h [NiFe] hydrogenase is accountable for atmospheric H2 oxidation and that it therefore could be a strong controlling factor in the global H2 cycle. We show that the isolated enzyme possesses a lower affinity (Km = 300 nM) for H2 than the membrane-associated enzyme. Hence, the membrane association seems essential for a high affinity for H2. The enzyme is extremely thermostable and remains folded up to 95 °C. Strain SolV is the only known organism in which the group 1h [NiFe] hydrogenase is responsible for rapid growth on H2 as sole energy source as well as oxidation of subatmospheric H2. The ability to conserve energy from H2 could increase fitness of verrucomicrobial methanotrophs in geothermal ecosystems with varying CH4 fluxes. We propose that H2 oxidation can enhance growth of methanotrophs in aerated methane-driven ecosystems. Group 1h [NiFe] hydrogenases could therefore contribute to mitigation of global warming, since CH4 is an important and extremely potent greenhouse gas.</p

Gene-Based Modeling of Methane Oxidation in Coastal Sediments: Constraints on the Efficiency of the Microbial Methane Filter

Methane is a powerful greenhouse gas that is produced in large quantities in marine sediments. Microbially mediated oxidation of methane in sediments, when in balance with methane production, prevents the release of methane to the overlying water. Here, we present a gene-based reactive transport model that includes both microbial and geochemical dynamics and use it to investigate whether the rate of growth of methane oxidizers in sediments impacts the efficiency of the microbial methane filter. We focus on iron- and methane-rich coastal sediments and, with the model, show that at our site, up to 10% of all methane removed is oxidized by iron and manganese oxides, with the remainder accounted for by oxygen and sulfate. We demonstrate that the slow growth rate of anaerobic methane-oxidizing microbes limits their ability to respond to transient perturbations, resulting in periodic benthic release of methane. Eutrophication and deoxygenation decrease the efficiency of the microbial methane filter further, thereby enhancing the role of coastal environments as a source of methane to the atmosphere

Methanogenic archaea use a bacteria-like methyltransferase system to demethoxylate aromatic compounds

Methane-generating archaea drive the final step in anaerobic organic compound mineralization and dictate the carbon flow of Earth’s diverse anoxic ecosystems in the absence of inorganic electron acceptors. Although such Archaea were presumed to be restricted to life on simple compounds like hydrogen (H(2)), acetate or methanol, an archaeon, Methermicoccus shengliensis, was recently found to convert methoxylated aromatic compounds to methane. Methoxylated aromatic compounds are important components of lignin and coal, and are present in most subsurface sediments. Despite the novelty of such a methoxydotrophic archaeon its metabolism has not yet been explored. In this study, transcriptomics and proteomics reveal that under methoxydotrophic growth M. shengliensis expresses an O-demethylation/methyltransferase system related to the one used by acetogenic bacteria. Enzymatic assays provide evidence for a two step-mechanisms in which the methyl-group from the methoxy compound is (1) transferred on cobalamin and (2) further transferred on the C(1)-carrier tetrahydromethanopterin, a mechanism distinct from conventional methanogenic methyl-transfer systems which use coenzyme M as final acceptor. We further hypothesize that this likely leads to an atypical use of the methanogenesis pathway that derives cellular energy from methyl transfer (Mtr) rather than electron transfer (F(420)H(2) re-oxidation) as found for methylotrophic methanogenesis

Microbial Transformations of Nitrogen, Sulfur, and Iron Dictate Vegetation Composition in Wetlands: A Review

The majority of studies on rhizospheric interactions focus on pathogens, mycorrhizal symbiosis, or carbon transformations. Although the biogeochemical transformations of N, S, and Fe have profound effects on vegetation, these effects have received far less attention. This review, meant for microbiologists, biogeochemists, and plant scientists includes a call for interdisciplinary research by providing a number of challenging topics for future ecosystem research. Firstly, all three elements are plant nutrients, and microbial activity significantly changes their availability. Secondly, microbial oxidation with oxygen supplied by radial oxygen loss from roots in wetlands causes acidification, while reduction using alternative electron acceptors leads to generation of alkalinity, affecting pH in the rhizosphere, and hence plant composition. Thirdly, reduced species of all three elements may become phytotoxic. In addition, Fe cycling is tightly linked to that of S and P. As water level fluctuations are very common in wetlands, rapid changes in the availability of oxygen and alternative terminal electron acceptors will result in strong changes in the prevalent microbial redox reactions, with significant effects on plant growth. Depending on geological and hydrological settings, these interacting microbial transformations change the conditions and resource availability for plants, which are both strong drivers of vegetation development and composition by changing relative competitive strengths. Conversely, microbial composition is strongly driven by vegetation composition. Therefore, the combination of microbiological and plant ecological knowledge is essential to understand the biogeochemical and biological key factors driving heterogeneity and total (i.e., microorganisms and vegetation) community composition at different spatial and temporal scales

Dark carbon fixation in the Arabian Sea oxygen minimum zone contributes to sedimentary organic carbon (SOM)

In response to rising CO2concentrations and increasing global sea surface temperatures,oxygen minimum zones (OMZ), or“dead zones”, are expected to expand. OMZs are fueled by highprimary productivity, resulting in enhanced biological oxygen demand at depth, subsequent oxygen depletion, and attenuation of remineralization. This results in the deposition of organic carbon‐rich sediments. Carbon drawdown is estimated by biogeochemical models; however, a major process is ignored: carbon fixation in the mid‐and lower water column. Here, we show that chemoautotrophic carbon fixation is important in the Arabian Sea OMZ; and manifests in a13C‐depleted signature of sedimentary organic carbon. We determined theδ13C values of Corg deposited in close spatial proximity but over a steepbottom‐water oxygen gradient, and theδ13C composition of biomarkers of chemoautotrophic bacteriacapable of anaerobic ammonia oxidation (anammox). Isotope mixing models show that detritus fromanammox bacteria or other chemoautotrophs likely forms a substantial part of the organic matter depositedwithin the Arabian Sea OMZ (~17%), implying that the contribution of chemoautotrophs to settling organicmatter is exported to the sediment. This has implications for the evaluation of past, and future, OMZs:biogeochemical models that operate on the assumption that all sinking organic matter is photosynthetically derived, without new addition of carbon, could significantly underestimate the extent of remineralization. Oxygen demand in oxygen minimum zones could thus be higher than projections suggest, leading to a more intense expansion of OMZs than expected

Anaerobic ammonium-oxidising bacteria: A biological source of the bacteriohopanetetrol stereoisomer in marine sediments

Bacterially-derived bacteriohopanepolyols (BHPs) are abundant, well preserved lipids in modern and paleo-environments. Bacteriohopanetetrol (BHT) is a ubiquitously produced BHP while its less common stereoisomer (BHT isomer) has previously been associated with anoxic environments; however, its biological source remained unknown. We investigated the occurrence of BHPs in Golfo Dulce, an anoxic marine fjord-like enclosure located in Costa Rica. The distribution of BHT isomer in four sediment cores and a surface sediment transect closely followed the distribution of ladderane fatty acids, unique biomarkers for bacteria performing anaerobic ammonium oxidation (anammox). This suggests that BHT isomer and ladderane lipids likely shared the same biological source in Golfo Dulce. This was supported by examining the BHP lipid compositions of two enrichment cultures of a marine anammox species ('. Candidatus Scalindua profunda'), which were found to contain both BHT and BHT isomer. Remarkably, the BHT isomer was present in higher relative abundance than BHT. However, a non-marine anammox enrichment contained only BHT, which explains the infrequence of BHT isomer observations in terrestrial settings, and indicates that marine anammox bacteria are likely responsible for at least part of the environmentally-observed marine BHT isomer occurrences. Given the substantially greater residence time of BHPs in sediments, compared to ladderanes, BHT isomer is a potential biomarker for past anammox activity

Draft Genome Sequence of a New Methanobacterium Strain Potentially Resistant to Bile Salts, Isolated from Deer Feces

Contains fulltext : 222125.pdf (publisher's version ) (Open Access

Metabolic modeling of denitrification in Agrobacterium tumefaciens: A tool to study inhibiting and activating compounds for the denitrification pathway

A metabolic network model for facultative denitrification was developed based on experimental data obtained with Agrobacterium tumefaciens. The model includes kinetic regulation at the enzyme level and transcription regulation at the enzyme synthesis level. The objective of this work was to study the key factors regulating the metabolic response of the denitrification pathway to transition from oxic to anoxic respiration and to find parameter values for the biological processes that were modeled. The metabolic model was used to test hypotheses that were formulated based on the experimental results and offers a structured look on the processes that occur in the cell during transition in respiration. The main phenomena that were modeled are the inhibition of the cytochrome c oxidase by nitric oxide (NO) and the (indirect) inhibition of oxygen on the denitrification enzymes. The activation of transcription of nitrite reductase and NO reductase by their respective substrates were hypothesized. The general assumption that nitrite and NO reduction are controlled interdependently to prevent NO accumulation does not hold for A. tumefaciens. The metabolic network model was demonstrated to be a useful tool for unraveling the different factors involved in the complex response of A. tumefaciens to highly dynamic environmental conditions.BT/BiotechnologyApplied Science