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were deduced from standard curves. OD600 was measured on a Beckman DU®640B spectrophotometer in plastic 1.5 mL cuvettes with a 1 cm path length.
RNA-seq
Two replicate cultures were grown to mid exponential phase (OD600 0.29 0.01) for approximately 24 h, then collected by pouring 45 mL of culture into 50 mL tubes containing 5 mL of stop solution comprised of 5% water-equilibrated phenol, pH 6.6 (Sigma; St. Louis, MO, USA), and 95% ethanol (200 Proof; Deacon Labs, Inc., King of Prussia, PA, USA). The cells were collected by centrifugation at 4,300 g at 4˚C for 10 min. The resultant pellet was re-suspended in 0.75 mL of extraction buffer [2.5% CTAB (Sigma; St. Louis, MO, USA), 0.7 M NaCl, and 0.075 M pH 7.6 phosphate buffer] and transferred to a 2 mL sterilized screw-cap tube containing 0.75 mL of phenol:chloroform:isoamylic alcohol with a volume ratio of 25:24:1 (Ambion®; Austin, TX, USA), 0.5 g of 0.1 mm silica beads (Biospec products; Bartlesville, OK, USA), 0.2% SDS (Ambion®; Austin, TX, USA), and 0.2% lauryl sarkosine (Sigma; St. Louis, MO, USA). The mixtures were homogenized in a bead beater (Mini-Beadbeater; Biospec Products; Bartlesville, OK, USA) for 2 min (75% of the maximum power). The resulting slurry was centrifuged for 5 min at 4˚C and 20,800 g. The aqueous layer was transferred to a fresh tube containing 0.75 mL of chloroform:isoamylic alcohol with a volumetric ratio of 24:1 (Sigma; St. Louis, MO, USA) and centrifuged again for 5 min at 4˚C and 20,800 g to remove dissolved phenol. The aqueous phase was transferred to a new tube. MgCl2 (final concentration 3 mM), sodium acetate (10 mM, pH 5.5), and 0.8 mL icecold isopropanol were added. Nucleic acids were transferred to 80˚C for overnight precipitation. Precipitated samples were centrifuged for 45 min at 4˚C and 14,000 RPM (20,800 g ), washed with 0.5 mL of 75% ethanol (made from 200 proof; Deacon Labs, Inc., King of Prussia, PA, USA), and dried for 15 min at room temperature.
An RNeasy Mini Kit (Qiagen©; Venlo, Netherlands) with two types of DNA digestions was used to isolate the mRNA. Initially, the DNA/RNA pellet was re-suspended in 80 mL of a DNase I (RNase-free) mixture (Ambion®; Austin, TX, USA) and incubated for 30 min at 37˚C. Then, the samples were purified on RNeasy Mini Kit columns as described in the RNA cleanup section of the manual, including the optional on-column DNAse digestion. The MICROBExpress™(Ambion®; Austin, TX, USA) kit was applied to each sample to reduce the rRNA concentration and increase the mRNA sequencing depth.
The sample quality was monitored with three techniques: (1) by electrophoresis in TAE buffer in 1% agarose gels (2) using an Agilent 2100 Bioanalyzer with Agilent RNA 6000 Nano-kit as suggested by the manufacturer, and (3) by real-time reversetranscriptase PCR (RT-RT PCR) with 16S rRNA (27F/536R) and pmoA-specific (Auman et al., 2001) primers.
TRANSCRIPT SEQUENCING, ALIGNMENT, AND MAPPING
Enriched RNA samples (i.e., two biological replicates) were submitted to the University of Washington’s High-Throughput Sequencing Solutions Center on dry ice for single-read Illumina®sequencing (Department of Genome Sciences, University of
Washington2). The replicates were aligned to the reference genome using BWA under default parameters (Li and Durbin, 2009). The “METTOv1” genome sequence was downloaded from MaGE (Vallenet et al., 2006). The single large pseudo scaffold distributed by MaGE was split into 187 separate contigs at each stretch of N bases. In addition, chimeric contigs from the assembly and low quality gene calls were removed (Table S5 in Supplementary Material). The summary of RNA-seq (Illumina) reads can be found in Table S4 in Supplementary Material. The METTOv1 genome did not have a complete pmoCAB cluster suitable for alignment. In order to include pmoCAB, a separate alignment run was performed with the previously published sequence of this gene cluster (Holmes et al., 1995). After the alignment with BWA, SAM tools was used to generate a pileup file that was loaded into a MySQL database for normalization from Reads Per Kilobase of gene per Million mapped reads (RPKM) to coding sequences (Mortazavi et al., 2008).
TRANSCRIPTION SITE MAPPING AND TRANSCRIPTOME BASED GENE ASSEMBLY
The reads mapped at each base position in the genomic scaffolds generated from the pileup were manually examined to identify putative transcription starts and stops. Briefly, reads mapped per base data for the two replicates were plotted on a log scale. The boundary of a rapid transition from near zero reads mapped to 10, 100 RPKM or more that was upstream of a gene start was designated a transcription start. Stops were similarly identified as a rapid transition to low numbers of reads mapped downstream of a gene termination codon.
Given the fragmented nature of the M. trichosporium OB3b genome, we performed de novo assembly of the RNA-Seq reads, in an attempt to identify transcripts whose genomic sequences were incomplete. The assembly was performed with Velvet 1.2.06 (Zerbino and Birney, 2008) and Oases 0.2.08 (Schulz et al., 2012). The oases pipeline tool distributed with Oases was used to survey assemblies across the range of odd k-mers from 17 to 35 where the minimum fragment length was set to 100 bp. The final merged assembly from the pipeline tool was stripped down to the highest confidence transcript for each locus with confidence ties resolved by taking the longest sequence. The high confidence assembled transcripts were aligned to the M. trichosporium OB3b scaffolds using BLASTn. Transcripts without significant matches were aligned with BLASTx to the protein non-redundant database, as retrieved on January 13, 2012.
ACKNOWLEDGMENTS
This project was funded by the DOE (DE-SC0005154). Authors are very grateful to Mary E. Lidstrom, Ludmila Chistoserdova, and Valentina N. Khmelenina for many insightful suggestions on the manuscript.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at http://www.frontiersin.org/Microbiological_Chemistry/10.3389/ fmicb.2013.00040/abstract
2http://www.htseq.org/
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Figure S1 | RNA-Seq reads mapped per base relative to start of pmo-operon. Left, the average number of reads mapped to the region 330 to 270 upstream from the start of pmoC for two biological replicates. The sequence at each base is shown above the bars. Right, the range (shown in red) and mean of two biological replicates (shown as black line) for the number of reads mapped per base for the coding and downstream region of the pmo-operon.
Figure S2 | Genetic organization and relative expression (RPKM) of the mxa gene cluster (A), the pqq gene cluster (B) and cluster of genes encoding reactions of the H4 MPT-linked C1 transfer pathway (C).
Figure S3 | RNA-Seq reads mapped per base relative to start of mxaF ORF.
Left, the average number of reads mapped to the region 200 to 140 upstream from the start of mxaF for two biological replicates. The sequence at each base is shown above the bars. Right, the range (shown in red) and mean of two biological replicates (shown as black line) for the number of reads mapped per base for the coding and downstream region of the mxaF cluster.
Figure S4 | RNA-Seq reads mapped per base relative to start of serine cycle gene operon. The log10 average number of reads mapped at each base from biological replicates one and two is shown. In (A), the upstream location spanning 250 to 190 from putative start of ftfL. (B) The expression over the entire operon. Note the several drop to near zero upstream indicating the operon is not co-transcribed. (C) The 230 to 170 region upstream from sga.
REFERENCES
Anthony, C. (1978). The prediction of growth yields in methylotrophs. J. Gen. Microbiol. 104, 91–104.
Anthony, C. (1982). The Biochemistry of Methylotrophs. New York: Academic Press Inc.
Anthony, C. (2002). Methanol dehydrogenase, a PQQ-containing quinoprotein dehydrogenase.
Subcell. Biochem. 35, 73–117. Anthony, C. (2011). How half a century
of research was required to understand bacterial growth on C1 and C2 compounds; the story of the serine cycle and the ethylmalonyl-CoA pathway. Sci. Prog. 94, 109–137.
Anthony, C., Ghosh, M., and Blake, C. C. (1994). The structure and function of methanol dehydrogenase and related quinoproteins containing pyrrolo-quinoline quinone. Biochem. J. 304, 665–674.
Auman, A. J., Speake, C. C., and Lidstrom, M. E. (2001). nifH sequences and nitrogen fixation in type I and type II methanotrophs. Appl. Environ. Microbiol. 67, 4009–4016.
Balasubramanian, R., and Rosenzweig, A. C. (2008). Copper methanobactin: a molecule whose time has come. Curr. Opin. Chem. Biol. 12, 245–249.
Balasubramanian, R., Smith, S. M., Rawat, S., Yatsunyk, L. A., Stemmler, T. L., and Rosenzweig, A. C. (2010). Oxidation of methane by a biological dicopper centre. Nature 465, 115–119.
Berube, P. M., and Stahl, D. A. (2012). The divergent AmoC3 subunit of ammonia monooxygenase functions as part of a stress response system in
Nitrosomonas europaea. J. Bacteriol.
189, 3448–3456. |
|
|
|
||
Caccamo, |
M. |
A., |
Malone, |
C. |
M., |
and |
Rasche, |
M. E. |
(2004). |
||
Biochemical |
|
characterization |
|||
of |
a |
dihydromethanopterin |
|||
reductase involved in tetrahy- |
|||||
dromethanopterin biosynthesis |
in |
||||
Methylobacterium extorquens AM1.
J. Bacteriol. 186, 2068–2073.
Chen, Y., Crombie, A., Rahman, M. T., Dedysh, S. N., Liesack, W., Stott, M. B., et al. (2010). Complete genome sequence of the aerobic facultative methanotroph Methylocella silvestris BL2. J. Bacteriol. 192, 3840–3841.
Chistoserdova, L. (2011). Modularity of methylotrophy, revisited. Environ. Microbiol. 13, 2603–2622.
Chistoserdova, L., Kalyuzhnaya, M. G., and Lidstrom, M. E. (2009). The expanding world of methylotrophic metabolism. Annu. Rev. Microbiol.
63, 477–499. |
|
|
|
Chistoserdova, L., |
Rasche, |
M. E., |
|
and Lidstrom, |
M. |
E. |
(2005). |
Novel |
dephosphotetrahy- |
||
dromethanopterin |
biosynthesis |
||
genes discovered via mutagenesis in
Methylobacterium extorquens AM1.
J. Bacteriol. 187, 2508–2512. Chistoserdova, L., Vorholt, J. A., Thauer,
R. K., and Lidstrom, M. E. (1998). C1 transfer enzymes and coenzymes linking methylotrophic bacteria and
Bases from the Cstrand are shown across the top of the figure. (D) The 270 to 210 region upstream of mclA.
Figure S5 | RNA-Seq reads mapped per base relative to start of fae1-1. Left, the average number of reads mapped to the region 235 to 185 upstream from the start of fae1-1 gene for two biological replicates. The sequence at each base is shown above the bars. Right, the range (shown in red) and mean of two biological replicates (shown as black line) for the number of reads mapped per base for the coding and downstream region of the fae1-1 and fae1-2 genes.
Figure S6 | Primary structure alignment for phosphoenolpyruvate carboxylases (Ppc1 and Ppc2) from M. trichosporium OB3b and Ppc-homologs.
Table S1 | Transcripts detected by de novo assembly RNA-Seq data.
Table S2 | Gene expression profile in methane-grown cells of M. trichosporium OB3b. Values represent reads per kilobase of coding sequence per million (reads) mapped (RPKM).
Table S3 | Summary of putative transcription site mapping (Note that the published sequences need references added).
Table S4 | Summary of RNA-seq (Illumina) reads.
Table S5 | Genes removed from reference scaffold before alignment.
methanogenic archaea. Science 281, 99–102.
Chu, K. H., and Alvarez-Cohen, L. (1998). Effect of nitrogen source on growth and trichloroethylene degradation by methane-oxidizing bacteria. Appl. Environ. Microbiol.
64, 3451–3457.
Crowther, G. J., Kosály, G., and Lidstrom, M. E. (2008). Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J. Bacteriol. 190, 5057–5062.
Dam, B., Kube, M., Dam, S., Reinhardt, R., and Liesack, W. (2012a). Complete sequence analysis of two methanotroph-specific repABC-containing plasmids from
Methylocystis sp. strain SC2. Appl. Environ. Microbiol. 78, 4373–4379.
Dam, B., Dam, S., Kube, M., Reinhardt, R., and Liesack, W. (2012b). Complete genome sequence of Methylocystis sp. strain SC2, an aerobic methanotroph with high-affinity methane oxidation potential. J. Bacteriol. 194, 6008–6009.
Doronina, N. V., Ezhov, V. A., and Trotsenko, Yu. A. (2008). Growth of Methylosinus trichosporium
OB3b on methane and poly-beta- hydroxybutyrate biosynthesis. Prikl. Biokhim. Mikrobiol. 44, 182–185.
Dunfield, P. F., Yuryev, A., Senin, P., Smirnova, A. V., Stott, M. B., Hou, S., et al. (2007). Methane oxidation by an extremely acidophilic bacterium of the phylumVerrucomicrobia. Nature 450, 879–882.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797.
Elango, N., Radhakrishnan, R., Froland, W. A., Wallar, B. J., Earhart, C. A., Lipscomb, J. D., et al. (1997). Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci. 6, 556–568.
EPA. (1993). Emerging Technology Summary Pilot-Scale Demonstration of a Two-Stage Methanotrophic Bioreactor for Biodegradation of Trichloroethylene in Groundwater. Available at: http://nepis.epa.gov
Fitch, M. W., Speitel, G. E., and Georgiou, G. (1996). Degradation of trichloroethylene by methanolgrown cultures of Methylosinus trichosporium OB3b PP358. Appl. Environ. Microbiol. 62, 1124–1128.
Gilbert, B., McDonald, I. R., Finch, R., Stafford, G. P., Nielsen, A. K., and Murrell, J. C. (2000). Molecular analysis of the pmo (particulate methane monooxygenase) operons from two type II methanotrophs. Appl. Environ. Microbiol.
66, 966–975.
Guckert, J. B., Ringelberg, D. B., White, D. C., Hanson, R. S., and Bratina, B. J. (1991). Membrane fatty acids as phenotypic markers in the polyphasic taxonomy of methylotrophs within the Proteobacteria. J. Gen. Microbiol. 137, 2631–2641.
Frontiers in Microbiology | Microbiological Chemistry |
April 2013 | Volume 4 | Article 40 | 14 |
Matsen et al. |
Methane utilization pathways in M. trichosporium OB3b |
|
|
Hakemian, A. S., Kondapalli, K. C., Telser, J., Hoffman, B. M., Stemmler, T. L., and Rosenzweig, A. C. (2008). The metal centers of particulate methane monooxygenase from
Methylosinus |
trichosporium OB3b. |
|
Biochemistry 47, 6793–6801. |
||
Hakemian, A. |
S., and |
Rosenzweig, |
A. C. (2007). The |
biochemistry |
|
of methane oxidation. Annu. Rev. Biochem. 76, 223–241.
Hanson, R. S., and Hanson, T. E. (1996). Methanotrophic bacteria. Microbiol. Rev. 60, 439–471.
Higgins, I. J., Best, D. J., Hammond, R. C., and Scott, D. (1981). Methaneoxidizing microorganisms. Microbiol. Rev. 45, 556–590.
Holmes, A. J., Costello, A., Lidstrom, M. E., and Murrell, J. C. (1995). Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132, 203–208.
Hou, C. T., Patel, R., Laskin, A. I., and Barnabe, N. (1979). Microbial oxidation of gaseous hydrocarbons: epoxidation of C2 to C4 n-alkenes by methylotrophic bacteria. Appl. Environ. Microbiol. 38,
127–134. |
|
Hou, S., Makarova, K. S., |
Saw, J. |
H., Senin, P., Ly, B. V., Zhou, Z., |
|
et al. (2008). Complete |
genome |
sequence of the extremely acidophilic methanotroph isolate V4,
Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol. Direct 3, 26.
Jollie, D. R., and Lipscomb, J. D. (1991). Formate dehydrogenase from
Methylosinus trichosporium OB3b. Purification and spectroscopic characterization of the cofactors. J. Biol. Chem. 266, 21853–21863.
Kai, |
Y., Matsumura, H., and Izui, |
|
K. |
(2003). |
Phosphoenolpyruvate |
carboxylase: |
three-dimensional |
|
structure and molecular mechanisms. Arch. Biochem. Biophys. 414, 170–179.
Kalyuzhnaya, M. G., Korotkova, N., Crowther, G., Marx, C. J., Lidstrom, M. E., and Chistoserdova, L. (2005). Analysis of gene islands involved in methanopterin-linked C1 transfer reactions reveals new functions and provides evolutionary insights. J. Bacteriol. 187, 4607–4614.
Karsten, W. E., Ohshiro, T., Izumi, Y., and Cook, P. F. (2001). Initial velocity, spectral, and pH studies of the serine-glyoxylate aminotransferase from Hyphomicrobiuim methylovorum. Arch. Biochem. Biophys. 388, 267–275.
Kelly, D. P., Anthony, C., and Murrell, J. C. (2005). Insights into the obligate methanotroph Methylococcus capsulatus. Trends Microbiol. 13, 195–198.
Khadem, A. F., Pol, A., Wieczorek, A., Mohammadi, S. S., Francoijs, K. J., Stunnenberg, H. G., et al. (2011). Autotrophic methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicum SolV uses the Calvin-Benson-Bassham cycle for carbon dioxide fixation. J. Bacteriol. 193, 4438–4446.
Kim, H. J., and Graham, D. W. (2001). Effect of oxygen level on simultaneous nitrogenase and sMMO expression and activity in Methylosinus trichosporium OB3b and its sMMoC mutant, PP319: aerotolerant N2 fixation in PP319. FEMS Microbiol. Lett. 201, 133–138.
Kim, H. J., Graham, D. W., DiSpirito, A. A., Alterman, M. A., Galeva, N., Larive, C. K., et al. (2004). Methanobactin, a copperacquisition compound from methane-oxidizing bacteria. Science 305, 1612–1615.
Krentz, B. D., Mulheron, H. J., Semrau, J. D., Dispirito, A. A., Bandow, N. L., Haft, D. H., et al. (2010). A comparison of methanobactins from
Methylosinus trichosporium OB3b and Methylocystis strain Sb2 predicts methanobactins are synthesized from diverse peptide precursors modified to create a common core for binding and reducing copper ions. Biochemistry 49, 10117–10130.
Large, P. J., and Quayle, J. R. (1963). Microbial growth on C(1) compounds. 5. Enzyme activities in extracts of Pseudomonas AM1. Biochem. J. 87, 386–396.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
Lawrence, A. J., and Quayle, J. R. (1970). Alternative carbon assimilation pathways in methane-utilizing bacteria. J. Gen. Microbiol. 63, 371–374.
Letunic, I., and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128.
Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760.
Liepman, A. H., and Olsen, L. J. (2001). Peroxisomal alanine: glyoxylate aminotransferase (AGT1)
is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J. 25, 487–498.
Lloyd, J. S., Finch, R., Dalton, H., and Murrell, J. C. (1999). Homologous expression of soluble methane monooxygenase genes in Methylosinus trichosporium OB3b. Microbiology 145, 461–470.
Matsumura, H., Xie, Y., Shirakata, S., Inoue, T., Yoshinaga, T., Ueno, Y., et al. (2002). Crystal structures of C4 form maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10, 1721–1730.
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq.
Nat. Methods 5, 621–628.
Murrell, C. J., and Dalton, H. (1983a). Ammonia assimilation in Methylococcus capsulatus (Bath) and other obligate methanotrophs. Microbiology 129, 1197–1206.
Murrell, J. C., and Dalton, H. (1983b). Purification and properties of glutamine synthetase from Methylococcus capsulatus (Bath). J. Gen. Microbiol.
129, 1187–1196. |
|
|
Murrell, J. |
C., and Jetten, M. |
S. |
M. (2009). The microbial methane |
||
cycle. Environ. Microbiol. Rep. 1, |
||
279–284. |
|
|
Murrell, J. C., McDonald, I. R., and |
||
Gilbert, |
B. (2000). Regulation |
of |
expression of methane monooxygenases by copper ions. Trends Microbiol. 8, 221–225.
Naguib, M. (1979). Alternative carboxylation reactions in type II methylotrophs and the localization of carboxylase activities in the intracytoplasmic membranes. Z. Allg. Mikrobio. 19, 333–342.
Newaz, S. S., and Hersh, L. B. (1975). Reduced nicotinamide adenine dinucleotide-activated phosphoenolpyruvate carboxylase in Pseudomonas MA: potential regulation between carbon assimilation and energy production. J. Bacteriol. 124, 825–833.
Nielsen, A. K., Gerdes, K., and Murrell, J. C. (1997). Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium. Mol. Microbiol. 25, 399–409.
Oakley, C. J., and Murrell, J. C. (1988). nifH genes in the obligate methane oxidizing bacteria. FEMS Micriobiol. Lett. 49, 53–57.
Oldenhuis, R., Oedzes, J. Y., van der
Waarde, J. |
J., and |
Janssen, D. |
B. (1991). |
Kinetics of |
chlorinated |
hydrocarbon degradation by Methylosinus trichosporium OB3b and toxicity of trichloroethylene. Appl. Environ. Microbiol. 57, 7–14.
Park, S., Hanna, L. M., Taylor, R. T., and Droege, M. W. (1991). Batch cultivation of Methylosinus trichosporium OB3b. I: production of soluble methane monooxygenase. Biotechnol. Bioeng. 38, 423–433.
Park, S., Shah, N. N., Taylor, R. T., and Droege, M. W. (1992). Batch cultivation of Methylosinus trichosporium
OB3b: II. production of particulate methane monooxygenase. Biotechnol. Bioeng. 40, 151–157.
Patel, R. N., Hoare, S. L., and Hoare, D. S. (1979). (14C) acetate assimilation by obligate methylotrophs,
Pseudomonas methanica and Methylosinus trichosporium. Antonie Van Leeuwenhoek 45, 499–511.
Patel, R. N., Hou, C. T., Derelanko, P., and Felix, A. (1980). Purification and properties of a heme-containing aldehyde dehydrogenase from Methylosinus trichosporium. Arch. Biochem. Biophys. 203, 654–662.
Peyraud, R., Kiefer, P., Christen, P., Massou, S., Portais, J. C., and Vorholt, J. A. (2009). Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc. Natl. Acad. Sci. U.S.A. 106, 4846–4851.
Phelps, P. A.,Agarwal, S. K., Speitel, G. E. Jr., and Georgiou, G. (1992). Methylosinus trichosporium OB3b mutants having constitutive expression of soluble methane monooxygenase in the presence of high levels of copper. Appl. Environ. Microbiol. 58, 3701–3708.
Pieja, A. J., Sundstrom, E. R., and Criddle, C. S. (2011). Poly-3- hydroxybutyrate metabolism in the type II methanotroph Methylocystis parvus OBBP. Appl. Environ. Microbiol. 77, 6012–6019.
Rasche, M. E., Havemann, S. A., and Rosenzvaig, M. (2004). Characterization of two methanopterin biosynthesis mutants of Methylobacterium extorquens AM1 by use of a tetrahydromethanopterin bioassay. J. Bacteriol. 5, 1565–1570.
Reshetnikov, A. S., Rozova, O. N., Khmelenina, V. N., Mustakhimov, I. I., Beschastny, A. P., Murrell, J. C., et al. (2008). Characterization of the pyrophosphate-dependent 6- phosphofructokinase from Methylococcus capsulatus Bath. FEMS Microbiol. Lett. 288, 202–210.
Rozova, O. N., Khmelenina, V. N., and Trotsenko, Y. A. (2012). Characterization of recombinant PPidependent 6-phosphofructokinases
www.frontiersin.org |
April 2013 | Volume 4 | Article 40 | 15 |
Matsen et al. |
Methane utilization pathways in M. trichosporium OB3b |
|
|
from Methylosinus trichosporium OB3b and Methylobacterium nodulans ORS 2060. Biochemistry Mosc.
77, 288–295.
Schmidt, S., Christen, P., Kiefer, P., and Vorholt, J. A. (2010). Functional investigation of methanol dehydrogenase-like protein XoxF in
Methylobacterium extorquens AM1.
Microbiology 156, 2575–2586. Schulz, M. H., Zerbino, D. R., Vingron,
M., and Birney, E. (2012). Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086–1092.
Schwartz, A. C., Gockel, G., Gross, J., Moritz, B., and Meyer, H. E. (2004). Relations and functions of dyelinked formaldehyde dehydrogenase from Hyphomicrobium zavarzinii revealed by sequence determination and analysis. Arch. Microbiol. 182, 458–466.
Semrau, J. D., DiSpirito, A. A., and Yoon, S. (2010). Methanotrophs and copper. FEMS Microbiol. Rev. 34, 496–531.
Shishkina, V. N., and Trotsenko, Y. A. (1979). Pathways of ammonia assimilation in obligate methane utilizers. FEMS Microbiol. Lett. 5, 187–191.
Shishkina, V. N., and Trotsenko, Y. A. (1982). Multiple enzymatic lesions in obligate methanotrophic bacteria.
FEMS Microbiol. Lett. 13, 237–242. Skovran, E., Palmer, A. D., Rountree,
A.M., Good, N. M., and Lidstrom, M. E. (2011). XoxF is required for expression of methanol dehydrogenase in Methylobacterium extorquens
AM1. J. Bacteriol. 193, 6032–6038.
Stein, L. Y., Bringel, F., DiSpirito, A. A., Han, S., Jetten, M. S., Kalyuzhnaya, M. G., et al. (2011). Genome sequence of the methanotrophic alphaproteobacterium Methylocystis sp. strain Rockwell (ATCC 49242). J. Bacteriol. 193, 2668–2669.
Stein, L. Y., Yoon, S., Semrau, J. D., Dispirito, A. A., Crombie, A., Murrell, J. C., et al. (2010). Genome
sequence of the obligate methan-
otroph |
Methylosinus trichosporium |
|
strain |
OB3b. J. |
Bacteriol. 192, |
6497–6498. |
|
|
Stolyar, S., |
Costello, |
A. M., Peeples, |
T. L., and Lidstrom, M. E. (1999). |
||
Role of multiple gene copies in par- |
||
ticulate |
methane |
monooxygenase |
activity in the methane-oxidizing bacterium Methylococcus capsulatus
Bath. Microbiology 145, 1235–1244. Strom, T., Ference, T., and Quayle, J.
R. (1974). The carbon assimilation pathways of Methylococcus capsu-
latus, Pseudomonas methanica, |
|||
and |
Methylosinus |
trichospo- |
|
rium |
(OB3B) |
during |
growth |
on |
methane. |
Biochemistry 144, |
|
465–476.
Takahashi, R., Ohmori, T., Watanabe, K., and Tokuyama, T. (1993). Phosphoenolpyruvate carboxylase of an ammonia-oxidizing chemoautotrophic bacterium, Nitrosomonas europaea ATCC 25978. J. Ferment. Bioeng. 76, 232–234.
Toyama, H., Chistoserdova, L., and Lidstrom, M. E. (1997). Sequence
analysis of |
pqq |
genes required |
for biosynthesis of pyrroloquino- |
||
line quinone |
in |
Methylobacterium |
extorquens AM1 and the purification of a biosynthetic intermediate.
Microbiology 143, 595–602. Trotsenko, Y. A. (1976). “Isolation and
characterization of obligate methanotrophic bacteria,” in Microbial Production and Utilization of Gases, eds H. G. Schlegel, G. Gottschalk, and N. Pfennig (Gottingen: Goltze), 329–336.
Trotsenko, Y. A., and Murrell, J. C. (2008). Metabolic aspects of aerobic obligate methanotrophy. Adv. Appl. Microbiol. 63, 183–229.
Vallenet, D., Labarre, L., Rouy, Z., Barbe, V., Bocs, S., Cruveiller, S., et al. (2006). MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 10, 53–65.
Vorholt, J. A., Chistoserdova, L., Stolyar, S. M., Thauer, R. K., and
Lidstrom, M. E. (1999). Distribution of tetrahydromethanopterindependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J. Bacteriol. 181, 5750–5757.
Vorholt, J. A., Marx, C. J., Lidstrom, M. E., and Thauer, R. K. (2000). Novel formaldehyde-activating enzyme in
Methylobacterium extorquens AM1 required for growth on methanol. J. Bacteriol. 182, 6645–6650.
Wadzink, A. M., and Ribbons, D. W. (1975). Utilization of acetate by
Methanomonas methanooxidans. J. Bacteriol. 123, 380–381.
Ward, N., Larsen, O., Sakwa, J., Bruseth,
L., |
Khouri, H., Durkin, |
A. S., |
et |
al. (2004). Genomic |
insights |
into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol. 2:e303. doi:10.1371/journal.pbio.0020303
Weaver, T. L., Patrick, M. A., and Dugan, P. R. (1975). Whole-cell and membrane lipids o the methanotrophic bacterium Methylosinus trichosporium. J. Bacteriol. 124, 602–605.
Whittenbury, R., Phillips, K. C., and Wilkinson, J. F. (1970). Enrichment, isolation and some properties of methane-utilizing bacteria. J. Gen. Microbiol. 61, 205–218.
Williams, A. M. (1988). The Biochemistry and Physiology of Poly- beta-Hydroxybutyrate Metabolism in Methylosinus trichosporium OB3b. Ph.D. thesis, Biotechnology Centre, Cranfield Institute of Technology, Cranfield.
Wilson, S. M., Gleisten, M. P., and Donohue, T. J. (2008). Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides. Microbiology 154, 296–305.
Yamada, K., Shimoda, M., and Okura, I. (1991). Purification and characterization of methanol dehydrogenase from Methylosinus trichosporium (OB3b). J. Mol. Catal. 73, 381–386.
Yang, S., Matsen, J. B., Konopka, M., Green-Saxena, A., Clubb, J., Sadilek, M., et al. (2013). Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium
OB3b. Part II. Metabolomics and 13C-labeling study. Front. Microbiol. 4:70 doi:10.3389/fmicb. 2013.00070
Yoon, S., Kraemer, S. M., DiSpirito, A. A., and Semrau, J. D. (2010). An assay for screen microbial cultures for chalkophore production. Environ. Microbiol. 2, 295–303.
Zerbino, D. R., and Birney, E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829.
Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Received: 01 January 2013; paper pending published: 28 January 2013; accepted: 17 February 2013; published online: 03 April 2013.
Citation: Matsen JB, Yang S, Stein LY, Beck D and Kalyuzhnaya MG (2013) Global molecular analyses of methane metabolism in methanotrophic alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: transcriptomic study. Front. Microbiol. 4:40. doi:10.3389/fmicb.2013.00040
This article was submitted to Frontiers in Microbiological Chemistry, a specialty of Frontiers in Microbiology.
Copyright © 2013 Matsen, Yang , Stein, Beck and Kalyuzhnaya. This is an openaccess article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
Frontiers in Microbiology | Microbiological Chemistry |
April 2013 | Volume 4 | Article 40 | 16 |