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High Frequency of Phylogenetically Diverse Reductive Dehalogenase-Homologous Genes in Deep Subseafloor Sedimentary Metagenomes

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High Frequency of Phylogenetically Diverse Reductive Dehalogenase-Homologous Genes in Deep Subseafloor Sedimentary Metagenomes View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector ORIGINAL RESEARCH ARTICLE published: 03 March 2014 doi: 10.3389/fmicb.2014.00080 High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes Mikihiko Kawai 1,2, Taiki Futagami 1,3, Atsushi Toyoda 4, Yoshihiro Takaki 2, Shinro Nishi 2, Sayaka Hori 2, Wataru Arai 2, Taishi Tsubouchi 2, Yuki Morono 1,5, Ikuo Uchiyama 6,7, Takehiko Ito 8, Asao Fujiyama 4, Fumio Inagaki 1,5 and Hideto Takami 2* 1 Geomicrobiology Group, Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, Japan 2 Microbial Genome Research Group, Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan 3 Department of Bioscience and Biotechnology, Kyushu University, Fukuoka, Japan 4 Comparative Genomics Laboratory, Center for Information Biology, National Institute of Genetics, Mishima, Japan 5 Geobio-Engineering and Technology Group, Submarine Resources Research Project, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, Japan 6 National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Japan 7 Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, Okazaki, Japan 8 Department of Biological Sciences, Tokyo Institute of Technology, Yokohama, Japan Edited by: Marine subsurface sediments on the Pacific margin harbor diverse microbial communities Jennifer F.Biddle, University of even at depths of several hundreds meters below the seafloor (mbsf) or more. Previous Delaware, USA PCR-based molecular analysis showed the presence of diverse reductive dehalogenase Reviewed by: gene (rdhA) homologs in marine subsurface sediment, suggesting that anaerobic William D. Orsi, Woods Hole Oceanographic Institution, USA respiration of organohalides is one of the possible energy-yielding pathways in the Anne-Kristin Kaster, Stanford organic-rich sedimentary habitat. However, primer-independent molecular characterization University, USA of rdhA has remained to be demonstrated. Here, we studied the diversity and frequency *Correspondence: of rdhA homologs by metagenomic analysis of five different depth horizons (0.8, 5.1, Hideto Takami, Microbial Genome 18.6, 48.5, and 107.0 mbsf) at Site C9001 off the Shimokita Peninsula of Japan. From Research Group, Extremobiosphere Research Program, Institute of all metagenomic pools, remarkably diverse rdhA-homologous sequences, some of which Biogeosciences, Japan Agency for are affiliated with novel clusters, were observed with high frequency. As a comparison, we Marine-Earth Science and also examined frequency of dissimilatory sulfite reductase genes (dsrAB), key functional Technology, Natsushima 2-15, genes for microbial sulfate reduction. The dsrAB were also widely observed in the Yokosuka, Kanagawa, 237-0061, Japan metagenomic pools whereas the frequency of dsrAB genes was generally smaller than e-mail: [email protected] that of rdhA-homologous genes. The phylogenetic composition of rdhA-homologous genes was similar among the five depth horizons. Our metagenomic data revealed that subseafloor rdhA homologs are more diverse than previously identified from PCR-based molecular studies. Spatial distribution of similar rdhA homologs across wide depositional ages indicates that the heterotrophic metabolic processes mediated by the genes can be ecologically important, functioning in the organic-rich subseafloor sedimentary biosphere. Keywords: deep biosphere, dehalogenation, metagenome, rdhA, sedimentary habitat INTRODUCTION Ocean contribute significantly to the global subseafloor microbial Previous microbiological studies conducted in conjunction with biomass. scientific ocean drilling have demonstrated remarkably high In general, microbial activity in deep marine sediments, microbial cell abundance in deep and old organic carbon-rich regardless of location, is extraordinarily low because of the lim- marine subsurface sediments in the margins of the Pacific Ocean itation of bio-available electron donors and acceptors (D’Hondt (Parkes et al., 1994, 2000; Lipp et al., 2008). The biomass in the et al., 2004; Røy et al., 2012; Hoehler and Jørgensen, 2013). open Pacific Ocean sediments, where primary photosynthetic However, there are metabolically active and/or alive micro- production in the overlying water column is very small (e.g., bial populations in deep marine sediments. Using nano-scale South Pacific Gyre), is generally several orders of magnitude secondary ion-mass spectrometry (NanoSIMS), it has been lower than that in the marginal sedimentary areas (D’Hondt demonstrated that a large fraction of deep subseafloor micro- et al., 2009). The current estimate of the global subseafloor bial components are physiologically alive, i.e., incorporate sta- microbial biomass is 2.9 × 1029 cells, comprising ca. 0.6% of ble isotope-labeled carbon and nitrogen substrates (Morono the total carbon in living biomass on our planet (Kallmeyer et al., 2011). Successful extraction and sequencing of RNA and et al., 2012). These facts mean that microbial communities in visualization of RNA by fluorescent in situ hybridization have organic carbon-rich sediments in the margins of the Pacific also indicated the presence of metabolically active microbial www.frontiersin.org March 2014 | Volume 5 | Article 80 | 1 Kawai et al. rdhA homologs in subseafloor metagenome components in deep marine sediments (Schippers et al., 2005; In this study, we focused on the diversity, frequency and Sørensen and Teske, 2006; Mills et al., 2012; Orsi et al., 2013b). distribution of rdhA-homologs in organic carbon-rich marine In the deep subseafloor sedimentary biosphere, microbial subsurface sediments off the Shimokita Peninsula of Japan. The communities comprise phylogenetically diverse bacteria and samples used in this study were obtained during the Chikyu archaea (Inagaki et al., 2003, 2006; Teske, 2006; Fry et al., 2008), Shakedown Expedition CK06-06 in 2006 (Aoike, 2007), in which as well as eukaryotes (Orsi et al., 2013a)andviruses(Engelhardt relatively high cell numbers (>107 cells/cm3) were observed using et al., 2013; Yanagawa et al., 2013). Since the microbial con- an image-based cell count technique (Morono et al., 2009). stituents found in deep marine sediments are phylogenetically To obtain a comprehensive molecular overview of rdhA- distinct from known isolates, their metabolic and physiological homologous genes in marine subsurface sediments, we per- functions also remain largely unknown. In fact, the metagenomic formed metagenomic analysis of sediment core samples at five analysis of the Peru Margin sediments showed that a large fraction depths to 107 m below the seafloor. This study allowed us to (86–94%) of the sequences did not code any homologs of known quantitatively assess the metagenomic pools through primer- protein-coding genes (Biddle et al., 2008), suggesting that micro- independent phylogenetic analysis of rdhA-homologous genes, bial communities in marine subsurface are functionally and evo- extending our current knowledge of the functional and evolu- lutionarily quite distinct from other microbial ecosystems of the tional contexts of deep subseafloor microbial communities. Earth’s surface biosphere (Biddle et al., 2006, 2011). A genomic study of single cells isolated from marine subsurface sediments MATERIALS AND METHODS has revealed extracellular protein-degrading enzymes, suggesting SAMPLE COLLECTION that previously unidentified metabolic functions related to pro- Sediment samples used in this study were collected from Site tein degradation and recycling are present in the uncultured but C9001 Hole C (41◦ 10.6380 N, 142◦ 12.081 E), which is approx- predominant archaeal constituents in the marine subsurface sed- imately 80 km from the coast of Shimokita Peninsula, northeast- iments, such as members of the Miscellaneous Crenarchaeotic ern Japan, during the Chikyu Shakedown Expedition CK06-06 Group (Lloyd et al., 2013). In addition, stable isotope prob- in 2006 (Aoike, 2007). This site is at the same location of the ing of the benthic microbial community showed that archaeal Integrated Ocean Drilling Program (IODP) Expedition 337 hole membrane lipids are recycled for new biomass production with- designated as IODP Site C0020 Hole A (Inagaki et al., 2012). out energy-consuming lipid synthesis steps (Takano et al., 2010). The water depth at Site C9001 is 1180.5 m. The sample depths These observations consistently suggest that deep subseafloor examined in this metagenomic study are 0.8 (Core 1H-1), 5.1 microbial constituents have unique metabolic and physiologi- (Core 1H-4), 18.6 (Core 3H-2), 48.5 (Core 6H-3), and 107.0 cal functions that make them well suited for long-term survival (Core 12H-4) mbsf. Environmental parameters such as pore- under energy-limited conditions (Hoehler and Jørgensen, 2013). water chemistry and total organic carbon have been measured One of the possible electron-acceptor systems in anoxic (Aoike, 2007; Tomaru et al., 2009). After core recovery onboard marine sediments is an organohalide respiration pathway the vessel, 20-cm-long whole round scores were immediately (Bossert et al., 2003). Previous microbiological studies of var- sampled, and then the innermost part of the core was sub- ious terrestrial environments and isolates demonstrated that sampled using an autoclaved
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