Modularity of methylotrophy, revisited.
TL;DR: This review integrates the new findings from genomic analyses with the previously developed concept of modularity of methylotrophy, which indicates the existence of alternative enzymes/pathways for the specific metabolic goals of this phenomenon.
Abstract: Methylotrophy is a metabolic capability possessed by microorganisms that allows them to build biomass and to obtain energy from organic substrates containing no carbon-carbon bonds (C1 compounds, such as methane, methanol, etc.). This phenomenon in microbial physiology has been a subject of study for over 100 years, elucidating a set of well-defined enzymatic systems and pathways enabling this capability. The knowledge gained from the early genetic and genomic approaches to understanding methylotrophy pointed towards the existence of alternative enzymes/pathways for the specific metabolic goals. Different combinations of these systems in different organisms suggested that methylotrophy must be modular in its nature. More recent insights from genomic analyses, including the genomes representing novel types of methylotrophs, seem to reinforce this notion. This review integrates the new findings with the previously developed concept of modularity of methylotrophy.
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TL;DR: It was shown that lanthanides were essential as cofactor in a homodimeric MDH comparable with one of the MDHs of Methylobacterium extorquens AM1, and it was hypothesize that the Lanthanides provide superior catalytic properties to pyrroloquinoline quinone (PQQ)-dependent MDH, which is a key enzyme for both methanotrophics and methylotrophs.
Abstract: Summary
Growth of Methylacidiphilum fumariolicum SolV, an extremely acidophilic methanotrophic microbe isolated from an Italian volcanic mudpot, is shown to be strictly dependent on the presence of lanthanides, a group of rare earth elements (REEs) such as lanthanum (Ln), cerium (Ce), praseodymium (Pr) and neodymium (Nd). After fractionation of the bacterial cells and crystallization of the methanol dehydrogenase (MDH), it was shown that lanthanides were essential as cofactor in a homodimeric MDH comparable with one of the MDHs of Methylobacterium extorquens AM1. We hypothesize that the lanthanides provide superior catalytic properties to pyrroloquinoline quinone (PQQ)-dependent MDH, which is a key enzyme for both methanotrophs and methylotrophs. Thus far, all isolated MxaF-type MDHs contain calcium as a catalytic cofactor. The gene encoding the MDH of strain SolV was identified to be a xoxF-ortholog, phylogenetically closely related to mxaF. Analysis of the protein structure and alignment of amino acids showed potential REE-binding motifs in XoxF enzymes of many methylotrophs, suggesting that these may also be lanthanide-dependent MDHs. Our findings will have major environmental implications as metagenome studies showed (lanthanide-containing) XoxF-type MDH is much more prominent in nature than MxaF-type enzymes.
364 citations
Cites background from "Modularity of methylotrophy, revisi..."
...XoxFs are found in all available methylotroph genomes, but a clear role in methanol and/or formaldehyde oxidation has not been assigned as yet (Schmidt et al., 2010; Chistoserdova, 2011)....
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...…than MxaFtype MDHs and are present in all methylotrophs © 2013 John Wiley & Sons Ltd and Society for Applied Microbiology, Environmental Microbiology (Chistoserdova, 2011), it is tempting to speculate that besides the MDHs from strain SolV (this study) and Methylobacterium extorquens AM1…...
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...The occurrence of MxaF-type MDH in a phylogenetic tree as a subgroup in the XoxF-type enzymes (Chistoserdova, 2011) suggests that the latter type may be the primordial MDH....
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...The genome of the Methylophilaceae strain HTCC2181, a representative of this OM43 clade, was suggested to define a minimal gene set for methylotrophy and only possessed a XoxF type MDH (Giovannoni et al., 2008; Chistoserdova, 2011)....
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TL;DR: Future research is needed on metalloenzymes involved in the production of N2O 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.
Abstract: 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 CO2 cycling, fewer studies have explored metal requirements for microbial production and consumption of the second- and third-most abundant greenhouse gasses, methane (CH4) and nitrous oxide (N2O). Here we review the current state of biochemical, physiological and environmental research on transition metal requirements for microbial CH4 and N2O 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 “ANME” Archaea likely occurs via reverse methanogenesis since ANME possess most of the enzymes in the methanogenic pathway. Aerobic CH4 oxidation uses Cu or Fe for the first step depending on Cu availability, and additional Fe, Cu and Mo for later steps. N2O 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 N2O conversion to N2, have only been found in classical denitrifiers. Accumulation of N2O 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 newly-discovered pathway of N2O production by ammonia oxidizing Archaea, biological mechanisms for scavenging scarce metals, and possible links between metal bioavailability and greenhouse gas fluxes both in anaerobic environments where metals may be limiting due to sulfide-metal scavenging.
305 citations
Cites background or methods from "Modularity of methylotrophy, revisi..."
...For a more extensive discussion of the biochemistry of aerobic methanotrophy, the reader is referred to other reviews (Hanson and Hanson, 1996; Hakemian and Rosenzweig, 2007; Trotsenko and Murrell, 2008; Semrau et al., 2010; Chistoserdova, 2011)....
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...Approximately 50% of the CHOH produced by MDH/Mxa is assimilated into biomass, and the other half is further oxidized to formate (CHOOH) and then to CO2 to generate reducing equivalents (Hanson and Hanson, 1996; Trotsenko and Murrell, 2008; Chistoserdova, 2011)....
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TL;DR: The XoxF-MDHs described thus far are homodimeric proteins lacking the small subunit and possess a rare-earth element (REE) instead of calcium.
Abstract: Methanol dehydrogenase (MDH) catalyzes the first step in methanol use by methylotrophic bacteria and the second step in methane conversion by methanotrophs. Gram-negative bacteria possess an MDH with pyrroloquinoline quinone (PQQ) as its catalytic center. This MDH belongs to the broad class of eight-bladed β propeller quinoproteins, which comprise a range of other alcohol and aldehyde dehydrogenases. A well-investigated MDH is the heterotetrameric MxaFI-MDH, which is composed of two large catalytic subunits (MxaF) and two small subunits (MxaI). MxaFI-MDHs bind calcium as a cofactor that assists PQQ in catalysis. Genomic analyses indicated the existence of another MDH distantly related to the MxaFI-MDHs. Recently, several of these so-called XoxF-MDHs have been isolated. XoxF-MDHs described thus far are homodimeric proteins lacking the small subunit and possess a rare-earth element (REE) instead of calcium. The presence of such REE may confer XoxF-MDHs a superior catalytic efficiency. Moreover, XoxF-MDHs are able to oxidize methanol to formate, rather than to formaldehyde as MxaFI-MDHs do. While structures of MxaFI- and XoxF-MDH are conserved, also regarding the binding of PQQ, the accommodation of a REE requires the presence of a specific aspartate residue near the catalytic site. XoxF-MDHs containing such REE-binding motif are abundantly present in genomes of methylotrophic and methanotrophic microorganisms and also in organisms that hitherto are not known for such lifestyle. Moreover, sequence analyses suggest that XoxF-MDHs represent only a small part of putative REE-containing quinoproteins, together covering an unexploited potential of metabolic functions.
279 citations
Cites background or methods from "Modularity of methylotrophy, revisi..."
...Many species employ the tetrahydromethanopterin (H4MPT)-dependent route for formaldehyde oxidation (Chistoserdova et al. 1998; see for reviews, Chistoserdova et al. 2009; Chistoserdova 2011)....
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...All in all, the field of methano- and methylotrophy is a rapidly expanding puzzle of redundant anabolic and catabolic possibilities and opportunities (Chistoserdova et al. 2009; Chistoserdova 2011)....
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...For formate reduction, two different routes are available that both employ H4folate as the C-1 carrier (Table 2) (Chistoserdova et al. 2009; Chistoserdova 2011)....
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...Again, XoxF-MDHs are phylogenetically diverse and at least five clades can be distinguished (Chistoserdova 2011)....
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...2002), formate is oxidized to CO2 by one of the different formate dehydrogenases (FDH) that the bacteria have at their disposal (Chistoserdova 2011)....
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TL;DR: Biodiversity, catalytic properties and key enzymes and pathways of these microbes are summarized, and an analysis of raw material costs suggests that methane- derived diesel fuel has the potential to be competitive with petroleum-derived diesel.
258 citations
TL;DR: The analyses, providing no unequivocal evidence for the monophyly of roseobacters, indicate several shifts between marine and non-marine habitats that occurred independently and were accompanied by characteristic changes in genomic content of orthologs, enzymes and metabolic pathways.
Abstract: Marine Rhodobacteraceae (Alphaproteobacteria) are key players of biogeochemical cycling, comprise up to 30% of bacterial communities in pelagic environments and are often mutualists of eukaryotes. As 'Roseobacter clade', these 'roseobacters' are assumed to be monophyletic, but non-marine Rhodobacteraceae have not yet been included in phylogenomic analyses. Therefore, we analysed 106 genome sequences, particularly emphasizing gene sampling and its effect on phylogenetic stability, and investigated relationships between marine versus non-marine habitat, evolutionary origin and genomic adaptations. Our analyses, providing no unequivocal evidence for the monophyly of roseobacters, indicate several shifts between marine and non-marine habitats that occurred independently and were accompanied by characteristic changes in genomic content of orthologs, enzymes and metabolic pathways. Non-marine Rhodobacteraceae gained high-affinity transporters to cope with much lower sulphate concentrations and lost genes related to the reduced sodium chloride and organohalogen concentrations in their habitats. Marine Rhodobacteraceae gained genes required for fucoidan desulphonation and synthesis of the plant hormone indole 3-acetic acid and the compatible solutes ectoin and carnitin. However, neither plasmid composition, even though typical for the family, nor the degree of oligotrophy shows a systematic difference between marine and non-marine Rhodobacteraceae. We suggest the operational term 'Roseobacter group' for the marine Rhodobacteraceae strains.
232 citations
Cites background from "Modularity of methylotrophy, revisi..."
...For methylotrophic bacteria such as Paracoccus or Rhodobacter, formaldehyde is also a central intermediate for oxidizing methanol or methylamine (Ras et al., 1995; Harms et al., 1996; Barber et al., 1996; Chistoserdova, 2011)....
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References
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J. Craig Venter Institute1, University of Southern California2, University of California, Davis3, National Autonomous University of Mexico4, University of Hawaii5, Bedford Institute of Oceanography6, Smithsonian Tropical Research Institute7, University of Concepción8, University of Costa Rica9, Rutgers University10
TL;DR: A metagenomic study of the marine planktonic microbiota in which surface (mostly marine) water samples were analyzed as part of the Sorcerer II Global Ocean Sampling expedition, which yielded an extensive dataset consisting of 7.7 million sequencing reads.
Abstract: The world's oceans contain a complex mixture of micro-organisms that are for the most part, uncharacterized both genetically and biochemically. We report here a metagenomic study of the marine planktonic microbiota in which surface (mostly marine) water samples were analyzed as part of the Sorcerer II Global Ocean Sampling expedition. These samples, collected across a several-thousand km transect from the North Atlantic through the Panama Canal and ending in the South Pacific yielded an extensive dataset consisting of 7.7 million sequencing reads (6.3 billion bp). Though a few major microbial clades dominate the planktonic marine niche, the dataset contains great diversity with 85% of the assembled sequence and 57% of the unassembled data being unique at a 98% sequence identity cutoff. Using the metadata associated with each sample and sequencing library, we developed new comparative genomic and assembly methods. One comparative genomic method, termed "fragment recruitment," addressed questions of genome structure, evolution, and taxonomic or phylogenetic diversity, as well as the biochemical diversity of genes and gene families. A second method, termed "extreme assembly," made possible the assembly and reconstruction of large segments of abundant but clearly nonclonal organisms. Within all abundant populations analyzed, we found extensive intra-ribotype diversity in several forms: (1) extensive sequence variation within orthologous regions throughout a given genome; despite coverage of individual ribotypes approaching 500-fold, most individual sequencing reads are unique; (2) numerous changes in gene content some with direct adaptive implications; and (3) hypervariable genomic islands that are too variable to assemble. The intra-ribotype diversity is organized into genetically isolated populations that have overlapping but independent distributions, implying distinct environmental preference. We present novel methods for measuring the genomic similarity between metagenomic samples and show how they may be grouped into several community types. Specific functional adaptations can be identified both within individual ribotypes and across the entire community, including proteorhodopsin spectral tuning and the presence or absence of the phosphate-binding gene PstS.
1,982 citations
TL;DR: Evidence for a fourth pathway to produce oxygen is presented, possibly of considerable geochemical and evolutionary importance, and opens up the possibility that oxygen was available to microbial metabolism before the evolution of oxygenic photosynthesis.
Abstract: Only three biological pathways are known to produce oxygen: photosynthesis, chlorate respiration and the detoxification of reactive oxygen species. Here we present evidence for a fourth pathway, possibly of considerable geochemical and evolutionary importance. The pathway was discovered after metagenomic sequencing of an enrichment culture that couples anaerobic oxidation of methane with the reduction of nitrite to dinitrogen. The complete genome of the dominant bacterium, named ‘Candidatus Methylomirabilis oxyfera’, was assembled. This apparently anaerobic, denitrifying bacterium encoded, transcribed and expressed the well-established aerobic pathway for methane oxidation, whereas it lacked known genes for dinitrogen production. Subsequent isotopic labelling indicated that ‘M. oxyfera’ bypassed the denitrification intermediate nitrous oxide by the conversion of two nitric oxide molecules to dinitrogen and oxygen, which was used to oxidize methane. These results extend our understanding of hydrocarbon degradation under anoxic conditions and explain the biochemical mechanism of a poorly understood freshwater methane sink. Because nitrogen oxides were already present on early Earth, our finding opens up the possibility that oxygen was available to microbial metabolism before the evolution of oxygenic photosynthesis. A previously unknown pathway producing oxygen during anaerobic methane oxidation linked to nitrite and nitrate reduction has been found in microbes isolated from freshwater sediments in Dutch drainage ditches. The complete genome of the bacterium responsible for this reaction has been assembled, and found to contain genes for aerobic methane oxidation. The bacterium reduces nitrite via the recombination of two molecules of nitric oxide into nitrogen and oxygen, bypassing the familiar denitrification intermediate nitrous oxide. This discovery is relevant to nitrogen and methane cycling in the environment and, since nitrogen oxides arose early on Earth, raises the possibility that oxygen was available to microbes before the advent of oxygen-producing photosynthesis. In certain microbes, the anaerobic oxidation of methane can be linked to the reduction of nitrates and nitrites. Here it is shown that this occurs through the intermediate production of oxygen. This brings the number of known biological pathways for oxygen production to four, with implications for our understanding of life on the early Earth.
1,463 citations
TL;DR: This review summarizes what is known and unknown about AOM on earth and its key catalysts, the anaerobic methanotrophic archaea clades and their bacterial partners.
Abstract: Methane is the most abundant hydrocarbon in the atmosphere, and it is an important greenhouse gas, which has so far contributed an estimated 20% of postindustrial global warming. A great deal of biogeochemical research has focused on the causes and effects of the variation in global fluxes of methane throughout earth's history, but the underlying microbial processes and their key agents remain poorly understood. This is a disturbing knowledge gap because 85% of the annual global methane production and about 60% of its consumption are based on microbial processes. Only three key functional groups of microorganisms of limited diversity regulate the fluxes of methane on earth, namely the aerobic methanotrophic bacteria, the methanogenic archaea, and their close relatives, the anaerobic methanotrophic archaea (ANME). The ANME represent special lines of descent within the Euryarchaeota and appear to gain energy exclusively from the anaerobic oxidation of methane (AOM), with sulfate as the final electron accept...
1,373 citations
TL;DR: To improve the prediction of climate models, it is important to understand the mechanisms by which microorganisms regulate terrestrial greenhouse gas flux, which involves consideration of the complex interactions that occur between microorganisms and other biotic and abiotic factors.
Abstract: Microbial processes have a central role in the global fluxes of the key biogenic greenhouse gases (carbon dioxide, methane and nitrous oxide) and are likely to respond rapidly to climate change. Whether changes in microbial processes lead to a net positive or negative feedback for greenhouse gas emissions is unclear. To improve the prediction of climate models, it is important to understand the mechanisms by which microorganisms regulate terrestrial greenhouse gas flux. This involves consideration of the complex interactions that occur between microorganisms and other biotic and abiotic factors. The potential to mitigate climate change by reducing greenhouse gas emissions through managing terrestrial microbial processes is a tantalizing prospect for the future.
831 citations