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The Genome Characteristics and Predicted Function of Methyl-Group Oxidation Pathway in the Obligate Aceticlastic Methanogens, Methanosaeta Spp

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The Genome Characteristics and Predicted Function of Methyl-Group Oxidation Pathway in the Obligate Aceticlastic Methanogens, Methanosaeta Spp The Genome Characteristics and Predicted Function of Methyl-Group Oxidation Pathway in the Obligate Aceticlastic Methanogens, Methanosaeta spp. Jinxing Zhu1,2, Huajun Zheng3, Guomin Ai1, Guishan Zhang1, Di Liu4, Xiaoli Liu1, Xiuzhu Dong1* 1 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, People’s Republic of China, 2 Graduate School, Chinese Academy of Sciences, Beijing, People’s Republic of China, 3 Shanghai-MOST Key Laboratory of Health and Disease Genomics, Chinese National Human Genome Center at Shanghai, Shanghai, People’s Republic of China, 4 Information center, Institute of Microbiology, Chinese Academy of Sciences, Beijing, People’s Republic of China Abstract In this work, we report the complete genome sequence of an obligate aceticlastic methanogen, Methanosaeta harundinacea 6Ac. Genome comparison indicated that the three cultured Methanosaeta spp., M. thermophila, M. concilii and M. harundinacea 6Ac, each carry an entire suite of genes encoding the proteins involved in the methyl-group oxidation pathway, a pathway whose function is not well documented in the obligately aceticlastic methanogens. Phylogenetic analysis showed that the methyl-group oxidation-involving proteins, Fwd, Mtd, Mch, and Mer from Methanosaeta strains cluster with the methylotrophic methanogens, and were not closely related to those from the hydrogenotrophic methanogens. Quantitative PCR detected the expression of all genes for this pathway, albeit ten times lower than the genes for aceticlastic methanogenesis in strain 6Ac. Western blots also revealed the expression of fwd and mch, genes involved in methyl-group oxidation. Moreover, 13C-labeling experiments suggested that the Methanosaeta strains might use the pathway as a methyl oxidation shunt during the aceticlastic metabolism. Because the mch mutants of Methanosarcina barkeri or M. acetivorans failed to grow on acetate, we suggest that Methanosaeta may use methyl-group oxidation pathway to generate reducing equivalents, possibly for biomass synthesis. An fpo operon, which encodes an electron transport complex for the reduction of CoM-CoB heterodisulfide, was found in the three genomes of the Methanosaeta strains. However, an incomplete protein complex lacking the FpoF subunit was predicted, as the gene for this protein was absent. Thus, F420H2 was predicted not to serve as the electron donor. In addition, two gene clusters encoding the two types of heterodisulfide reductase (Hdr), hdrABC, and hdrED, respectively, were found in the three Methanosaeta genomes. Quantitative PCR determined that the expression of hdrED was about ten times higher than hdrABC, suggesting that hdrED plays a major role in aceticlastic methanogenesis. Citation: Zhu J, Zheng H, Ai G, Zhang G, Liu D, et al. (2012) The Genome Characteristics and Predicted Function of Methyl-Group Oxidation Pathway in the Obligate Aceticlastic Methanogens, Methanosaeta spp.. PLoS ONE 7(5): e36756. doi:10.1371/journal.pone.0036756 Editor: Arnold Driessen, University of Groningen, The Netherlands Received November 15, 2011; Accepted April 11, 2012; Published May 10, 2012 Copyright: ß 2012 Zhu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding was provided by the National Natural Science Foundation of China under grant no. 30621005 and 30830007 (www.nsfc.gov.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction In contrast, species of the other genus of aceticlastic methan- ogens Methanosaeta are obligately aceticlastic. As specialists, Methanogenic Archaea are the only organisms known to produce Methanosaeta strains possess a higher affinity for acetate than abundant CH4 for energy metabolism. Therefore, they exert a Methanosarcina stains and are favored in environments with low significant ecological impact on global carbon cycling. Cultured concentrations of acetate [7]. Hence, they are deemed the methanogens are categorized into four metabolic types based on principal players in aceticlastic methanogenesis in nature. methanogenic precursors, including hydrogenotrophic, methylo- Thus far, only three Methanosaeta species have been cultured. M. trophic, aceticlastic and methanol plus H2 methanogenesis [1]. harundinacea is a mesophilic species isolated from an upflow anaerobic Since an estimated two-thirds of the methane in nature is from sludge blanket reactor treating beer-manufacturing wastewater in acetate [2], aceticlastic methanogenesis makes a major contribu- Beijing [8]. To gain insight into the genetic background of the tion to global methane production. So far, the methanogens aceticlastic methanogens, the complete genome of M. harundinacea utilizing acetate for methanogenesis are confined to the order 6Ac was sequenced and compared to that of the two other species. In Methanosarcinales. The genus Methanosarcina (Msr.) consists of the addition to the other common genome characteristics among the most metabolically diverse methanogenic species, most of them three species, unexpectedly the methyl-group oxidation pathway conduct three types of methanogenic metabolism [3]. In general, was present in all three genomes. In methylotrophic methanogens, Methanosarcina strains have large genomes, e.g. 5.8 Mb for Msr. this pathway provides reducing equivalents for methanogenesis [9]. acetivorans, 4.8 Mb for Msr. barkeri and 4.1 Mb for Msr. mazei It also plays a role in the anaerobic oxidation of methane [10,11]. To [4,5,6], and are about two times larger than other sequenced understand the possible function of the pathway, in this study, the methanogen genomes. expression of the genes in the pathway was tested in M. harundinacea PLoS ONE | www.plosone.org 1 May 2012 | Volume 7 | Issue 5 | e36756 Methanosaeta Genome and Methyl-Group Oxidation Figure 1. Circular representation of the M. harundinacea genome. The circles show (innermost to outermost): (1) GC skew; (2)G+C content; (3) genes included in the genome of M. harundinacea but not in the genomes of M. concilii and M. thermophila;(4) genes involved in methane metabolism; (5) genes found in all the three Methanosaeta genomes; (6) core genes found in the methanogen genomes sequenced; (7) RNA genes, including tRNA (red) and rRNAs (yellow); (8) genes on the plus and minus strand, respectively. All the genes were colored by functional categories according to COG classification. doi:10.1371/journal.pone.0036756.g001 6Ac. The gene expression and the preliminary physiological study 2,353 coding sequences (CDSs) with an average length of 937 bp suggest that the methyl-group oxidation pathway can be used to in the chromosome, representing 85% of the entire genome. Of generate the extra reducing equivalents in the obligate aceticlastic the protein-coding genes, 69.7% of the CDSs (1,640) were methanogens. assigned to the functional categories of Cluster of Orthologous Groups (COG). Approximately 22.4% (528/2,353) of the chro- Results and Discussion mosomal gene products are hypothetical proteins, accounting for the majority of the M. harundinacea-specific genes (226/305) when General genome features of Methanosaeta species compared with other available Methanosarcinales genomes. The In this study, the complete genome of Methanosaeta harundinacea plasmid pH 6AC is 11,991 bp in length and carries 18 predicted 6Ac, which contains a single circular chromosome and a circular ORFs, with 16 of these encoding hypothetical proteins. plasmid designated as pH 6AC, was obtained. The chromosome is A genome sequence comparison analysis for the three 2,559,043 bp in length with an average G+C content of 60.6% Methanosaeta strains, M. concilii GP6, M. thermophila PT, and M. (Figure 1). It contains one rRNA operon (5S, 16S, and 23S), a harundiacea 6Ac, did not reveal an obvious colinearity. However, a distinct 7S rRNA gene, and 39 tRNA genes (Table 1). There are remarkable difference among the three Methanosaeta species was PLoS ONE | www.plosone.org 2 May 2012 | Volume 7 | Issue 5 | e36756 Methanosaeta Genome and Methyl-Group Oxidation Table 1. General genome features of the aceticlastic methanogens, Methanosaeta spp. and Methanosarcina spp. General Msa. harundinacea Msa. concilii Msa. thermophila Msr. acetivorans Msr. barkeri Msr. mazei GenBank accession no. CP003117 NC_015416 NC_008553 NC_003552 NC_007355 NC_00391 Size (bp) 2,559,043 3,008,626 1,879,471 5,751,492 4,837,408 4,096,345 G+C content (%) 60.63 51 53.5 42.7 39.2 41.5 Protein-coding genes 2,353 2,906 1,781 4,540 3,698 3,371 Coding Regions (%) 81 83 82 74 70 75 rRNA operons 1 2 2 3 3 3 tRNA genes 39 44 48 59 62 57 Plasmid 1 1 0 1 1 0 Abbreviations: Msa., Methanosaeta; Msr., Methanosarcina. doi:10.1371/journal.pone.0036756.t001 observed in terms of the genome sizes, resulting in the difference in motility and secretion, defense systems, and post-translational gene content (Table 1), with M. thermophila PT having the smallest modification (PTM). This is probably consistent with its hot niche, genome, and M. concilii having more genes in category of DNA where the biodiversity is relatively lower. replication, recombination and repair, which is contributed by the multiple copies of the genes
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