Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide

Fluxes of greenhouse gases to the atmosphere are heavily influenced by microbiological activity. Microbial enzymes involved in the production and consumption of greenhouse gases often contain metal cofactors. While extensive research has examined the influence of Fe bioavailability on microbial CO_2 cycling, fewer studies have explored metal requirements for microbial production and consumption of the second- and third-most abundant greenhouse gases, methane (CH_4), and nitrous oxide (N_2O). Here we review the current state of biochemical, physiological, and environmental research on transition metal requirements for microbial CH_4 and N_2O cycling. Methanogenic archaea require large amounts of Fe, Ni, and Co (and some Mo/W and Zn). Low bioavailability of Fe, Ni, and Co limits methanogenesis in pure and mixed cultures and environmental studies. Anaerobic methane oxidation by anaerobic methanotrophic archaea (ANME) likely occurs via reverse methanogenesis since ANME possess most of the enzymes in the methanogenic pathway. Aerobic CH_4 oxidation uses Cu or Fe for the first step depending on Cu availability, and additional Fe, Cu, and Mo for later steps. N_2O production via classical anaerobic denitrification is primarily Fe-based, whereas aerobic pathways (nitrifier denitrification and archaeal ammonia oxidation) require Cu in addition to, or possibly in place of, Fe. Genes encoding the Cu-containing N_2O reductase, the only known enzyme capable of microbial N_2O conversion to N_2, have only been found in classical denitrifiers. Accumulation of N_2O due to low Cu has been observed in pure cultures and a lake ecosystem, but not in marine systems. Future research is needed on metalloenzymes involved in the production of N_2O by enrichment cultures of ammonia oxidizing archaea, biological mechanisms for scavenging scarce metals, and possible links between metal bioavailability and greenhouse gas fluxes in anaerobic environments where metals may be limiting due to sulfide-metal scavenging

Multiple prebiotic metals mediate translation.

Today, Mg2+ is an essential cofactor with diverse structural and functional roles in life's oldest macromolecular machine, the translation system. We tested whether ancient Earth conditions (low O2, high Fe2+, and high Mn2+) can revert the ribosome to a functional ancestral state. First, SHAPE (selective 2'-hydroxyl acylation analyzed by primer extension) was used to compare the effect of Mg2+, Fe2+, and Mn2+ on the tertiary structure of rRNA. Then, we used in vitro translation reactions to test whether Fe2+ or Mn2+ could mediate protein production, and quantified ribosomal metal content. We found that (i) Mg2+, Fe2+, and Mn2+ had strikingly similar effects on rRNA folding; (ii) Fe2+ and Mn2+ can replace Mg2+ as the dominant divalent cation during translation of mRNA to functional protein; and (iii) Fe and Mn associate extensively with the ribosome. Given that the translation system originated and matured when Fe2+ and Mn2+ were abundant, these findings suggest that Fe2+ and Mn2+ played a role in early ribosomal evolution

Hydrogenation reactions of carbon on Earth: linking methane, margarine, and life

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McGlynn, S. E., Glass, J. B., Johnson-Finn, K., Klein, F., Sanden, S. A., Schrenk, M. O., Ueno, Y., & Vitale-Brovarone, A. Hydrogenation reactions of carbon on Earth: linking methane, margarine, and life. American Mineralogist, 105(5), (2020): 599-608, doi:10.2138/am-2020-6928CCBYNCND.Hydrogenation reactions are a major route of electron and proton flow on Earth. Interfacing geology and organic chemistry, hydrogenations occupy pivotal points in the Earth’s global geochemical cycles. Some examples of hydrogenation reactions on Earth today include the production and consumption of methane in both abiotic and biotic reactions, the reduction of protons in hydrothermal settings, and the biological synthesis and degradation of fatty acids. Hydrogenation reactions were likely important for prebiotic chemistry on the early Earth, and today serve as one of the fundamental reaction classes that enable cellular life to construct biomolecules. An understanding and awareness of hydrogenation reactions is helpful for comprehending the larger web of molecular and material inter-conversions on our planet. In this brief review we detail some important hydrogenation and dehydrogenation reactions as they relate to geology, biology, industry, and atmospheric chemistry. Such reactions have implications ranging from the suite of reactions on early Earth to industrial applications like the production of hydrocarbon fuel.S.E.M. is supported by NSF Award 1724300 and JSPS KAKENHI Grant JP18H01325. A.V.B. is supported by ANR T-ERC, CNRS INSU-SYSTER, and Rita Levi Montalcini by MIUR. J.B.G. is supported by NASA Exobiology Grant NNX14AJ87G and 80NSSC19K0477. F.K. is supported by NSF-OCE award 1634032 and 1427274. M.O.S. is supported by the NASA Astrobiology Institute Rock-Powered Life Grant NNA15BB02A

Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments

Microbes have obligate requirements for trace metals in metalloenzymes that catalyse important biogeochemical reactions. In anoxic methane- and sulphide-rich environments, microbes may have unique adaptations for metal acquisition and utilization because of decreased bioavailability as a result of metal sulphide precipitation. However, micronutrient cycling is largely unexplored in cold (≤ 10°C) and sulphidic (> 1 mM ΣH_(2)S) deep-sea methane seep ecosystems. We investigated trace metal geochemistry and microbial metal utilization in methane seeps offshore Oregon and California, USA, and report dissolved concentrations of nickel (0.5–270 nM), cobalt (0.5–6 nM), molybdenum (10–5600 nM) and tungsten (0.3–8 nM) in Hydrate Ridge sediment porewaters. Despite low levels of cobalt and tungsten, metagenomic and metaproteomic data suggest that microbial consortia catalysing anaerobic oxidation of methane (AOM) utilize both scarce micronutrients in addition to nickel and molybdenum. Genetic machinery for cobalt-containing vitamin B_(12) biosynthesis was present in both anaerobic methanotrophic archaea (ANME) and sulphate-reducing bacteria. Proteins affiliated with the tungsten-containing form of formylmethanofuran dehydrogenase were expressed in ANME from two seep ecosystems, the first evidence for expression of a tungstoenzyme in psychrophilic microorganisms. Overall, our data suggest that AOM consortia use specialized biochemical strategies to overcome the challenges of metal availability in sulphidic environments

Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes

This is the peer reviewed version of the following article: Bray, M.S., Wu, J., Padilla, C.C., Stewart, F.J., Fowle, D.A., Henny, C., Simister, R.L., Thompson, K.J., Crowe, S.A. and Glass, J.B. (2020), Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes. Environmental Microbiology Reports, 12: 49-57. https://doi.org/10.1111/1758-2229.12809, which has been published in final form at https://doi.org/10.1111/1758-2229.12809. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. This article may not be enhanced, enriched or otherwise transformed into a derivative work, without express permission from Wiley or by statutory rights under applicable legislation. Copyright notices must not be removed, obscured or modified. The article must be linked to Wiley’s version of record on Wiley Online Library and any embedding, framing or otherwise making available the article or pages thereof by third parties from platforms, services and websites other than Wiley Online Library must be prohibited.Electroactive type IV pili, or e-pili, are used by some microbial species for extracellular electron transfer. Recent studies suggest that e-pili may be more phylogenetically and structurally diverse than previously assumed. Here, we used updated aromatic density thresholds (≥9.8% aromatic amino acids, ≤22-aa aromatic gaps and aromatic amino acids at residues 1, 24, 27, 50 and/or 51, and 32 and/or 57) to search for putative e-pilin genes in metagenomes from diverse ecosystems with active microbial metal cycling. Environmental putative e-pilins were diverse in length and phylogeny, and included truncated e-pilins in Geobacter spp., as well as longer putative e-pilins in Fe(II)-oxidizing Betaproteobacteria and Zetaproteobacteria

Molybdenum geochemistry in a seasonally dysoxic Mo-limited lacustrine ecosystem

Lakes are important for storage of the essential micronutrient molybdenum (Mo) during its transfer from the continents to the oceans, but little is known about the major sources and sinks for Mo in lacustrine ecosystems. We studied Mo cycling in Castle Lake, a small subalpine lake in the Klamath-Siskiyou Mountains of Northern California underlain primarily by mafic and ultramafic rocks where primary productivity is limited by Mo bioavailability. The deeper water of the lake becomes dysoxic (9–90 μM dissolved oxygen) during the summer. This study was undertaken to identify the sources of Mo to Castle Lake and establish a Mo budget. We measured Mo concentrations in a suite of bulk solids (lake sediments, soils and bedrock) and aqueous samples (sediment porewaters, soil runoff, spring waters, snow and ice) from Castle Lake and its watershed. Lake sediments have elevated Mo (7–36 ppm) compared to soils and bedrock (0.2–2 ppm) and Mo/Al values were nearly two orders of magnitude higher than the crustal abundance. Sediment porewaters had higher Mo (4–15 nM) than lake water (2–4 nM), soil runoff (0.1–6.2 nM), snowmelt (⩽0.1 nM), lake ice (0.3–2.2 nM) and local spring waters (0.03–2.72 nM). Bulk lake sediments had negative δ^(98/95)Mo values, ranging from −0.5 to −1.0‰ (±0.1). We used the numerical model PROFILE to estimate the net reaction rate of Mo in the porewater. Model calculations ruled out diagenesis as a source of Mo to lake sediments; diagenetic Mo always represented ⩽5% of the total Mo content in sediment. We also ruled out dissolved Mo inputs from groundwater and watershed inflow as important sources of Mo. Two whole-lake experimental Mo additions in the 1960’s could have contributed a sizeable amount of Mo to the lake sediments, but only over a short period. Atmospheric deposition of anthropogenic Mo from extensive copper smelting that occurred south of Castle Lake from 1896 to 1919 and from major Californian urban centers today were negligible Mo sources. Mo flux from the sediments (0.4–0.5 nmol cm^(−2) yr^(−1)) was roughly equal to Mo fluxes from surface inflow and outflow, whereas Mo burial fluxes were significantly higher (11.5 nmol cm^(−2) yr^(−1)). Because dissolved Mo fluxes were minimal, and atmospheric Mo deposition was estimated to be a minor source of Mo (<1 nmol cm^(−2) yr^(−1)), the largest source of Mo is non-detrital particulate matter (∼12 nmol cm^(−2) yr^(−1)), likely a mixture of organic matter and Fe–Mn oxyhydroxides as supported by Mo isotopic data

Bridging Alone: Religious Conservatism, Marital Homogamy, and Voluntary Association Membership

This study characterizes social insularity of religiously conservative American married couples by examining patterns of voluntary associationmembership. Constructing a dataset of 3938 marital dyads from the second wave of the National Survey of Families and Households, the author investigates whether conservative religious homogamy encourages membership in religious voluntary groups and discourages membership in secular voluntary groups. Results indicate that couples’ shared affiliation with conservative denominations, paired with beliefs in biblical authority and inerrancy, increases the likelihood of religious group membership for husbands and wives and reduces the likelihood of secular group membership for wives, but not for husbands. The social insularity of conservative religious groups appears to be reinforced by homogamy—particularly by wives who share faith with husbands

Embedding the Ni-SOD mimetic Ni-NCC within a polypeptide sequence alters specificity of the reaction pathway

This document is the Accepted Manuscript version of a Published Work that appeared in final form in the Inorganic Chemistry, copyright © American Chemical Society after peer review and technical editing by the publisher. To access the final edited and published work see http://doi.org/10.1021/ic301175f.The unique metal abstracting peptide (MAP) asparagine-cysteine-cysteine (NCC) binds nickel in a square planar 2N:2S geometry and acts as a mimic of the enzyme nickel superoxide dismutase (Ni-SOD). The Ni-NCC tripeptide complex undergoes rapid, site-specific chiral inversion to DLD-NCC in the presence of oxygen. Superoxide scavenging activity increases proportionally with the degree of chiral inversion. Characterization of the NCC sequence within longer peptides with absorption, circular dichroism (CD), and magnetic CD (MCD) spectroscopies and mass spectrometry (MS) shows that the geometry of metal coordination is maintained, though the electronic properties of the complex are varied to a small extent due to bis-amide, rather than amine/amide, coordination. In addition, both the Ni-tripeptides and Ni-pentapeptides have a −2 charge. The study here demonstrates that the chiral inversion chemistry does not occur when NCC is embedded in a longer polypeptide sequence. Nonetheless, the superoxide scavenging reactivity of the embedded Ni-NCC module is similar to that of the chirally inverted tripeptide complex, which is consistent with a minor change in reduction potential for the Ni-pentapeptide. Together, this suggests that the charge of the complex could affect the SOD activity as much as a change in primary coordination sphere. In Ni-NCC and other Ni-SOD mimics, changes in chirality, superoxide scavenging activity, and oxidation of the peptide itself all depend on the presence of dioxygen or its reduced derivatives (e.g., superoxide), and the extent to which each of these distinct reactions occurs is ruled by electronic and steric effects that emenate from the organization of ligands around the metal center

Submarine volcanic morphology of the western Galapagos based on EM300 bathymetry and MR1 side-scan sonar

Author Posting. © American Geophysical Union, 2007. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geochemistry Geophysics Geosystems 8 (2007): Q03010, doi:10.1029/2006GC001464.A compilation of high-resolution EM300 multibeam bathymetric and existing MR1 side-scan sonar data was used to investigate the volcanic morphology of the flanks of the western Galápagos Islands. The data portray an assortment of constructional volcanic features on the shallow to deep submarine flanks of Fernandina, Isabela, and Santiago Islands, including rift zones and groups of cones that are considered to be the primary elements in constructing the archipelagic apron. Ten submarine rift zones were mapped, ranging in length from 5 to 20 km, comparable in length to western Canary Island rift zones but significantly shorter than Hawaiian submarine rift zones. A detailed analysis of the northwestern Fernandina submarine rift, including calculated magnetization from a surface-towed magnetic study, suggests that the most recent volcanism has focused at the shallow end of the rift. Small submarine volcanic cones with various morphologies (e.g., pointed, cratered, and occasionally breached) are common in the submarine western Galápagos both on rift zones and on the island flanks where no rifts are present. At depths greater than ∼3000 m, large lava flow fields in regions of low bathymetric relief have been previously identified as a common seafloor feature in the western Galápagos by Geist et al. (2006); however, their source(s) remained enigmatic. The new EM300 data show that a number of the deep lava flows originate from small cones along the mid-lower portion of the NW submarine rift of Fernandina, suggesting that the deep flows owe their origin, at least in part, to submarine rift zone volcanism.Data collected on TN188 was funded by NSF grant OCE0326148 and NOAA grant NA04OAR460009 to S.M.W. Support for data collected on previous multibeam and MR1 cruises was provided by NSF grants OCE9811504 and OCE0002461 (D.J.F.)