Nitrosopumilus maritimus genome reveals unique - de la Torre ...

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work was supported by the Department of Energy Microbial Genome Program, by National Science Foundation Microbial Interactions and Processes Grant MCB-0604448 (to D.A.S. and J.R.d.l.T.), by National Science Foundation Molecular and Cellular Biosciences Grant MCB-0920741 (to D.A.S.), by National Science Foundation Biological Oceanography Grants OCE-0623174 (to D.A.S.) 1. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean.Nature 409:507–510. 2. Agogué H, Brink M, Dinasquet J, Herndl GJ (2008) Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456:788–791. 3. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89: 5685–5689. 4. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149. 5. Venter JC, et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74. 6. 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(2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–1740. 6of6 | www.pnas.org/cgi/doi/10.1073/pnas.0913533107 Walker et al.
Supporting Information Walker et al. 10.1073/pnas.0913533107 SI Materials and Methods High-Molecular-Weight Genomic DNA Preparation. Two cultures of Nitrosopumilus maritimus strain SCM1 were grown as previously described in 500 mL of media in 1-L flasks (1). Cells from both cultures were harvested in late-exponential phase using Sterivex filters for one culture and a 0.1-μm filter for the other. Highmolecular-weight DNA was isolated as previously described using either agarose plugs (2) or a modified guanadinium thiocynate protocol (3). Cells from the Sterivex filter were resuspended in 1 mL of 2× STE buffer [1 M NaCl, 0.1 M EDTA (pH 8.0), 10 mM Tris (pH 8.0)], extracted from the filter, and mixed with 1 vol of 1% molten SeaPlaque LMP agarose (FMC). The mixture was cooled to 40 °C, immediately drawn into a 1-mL syringe, and placed on ice for 10 min. The agarose plug was mixed with 10 mL of lysis buffer, incubated at 37 °C for 1 h, and then transferred to 40 mL of ESP buffer (1% Sarkosyl–1 mg of Proteinase K per ml in 0.5 M EDTA). After incubation at 55 °C for 16 h, the solution was replaced with fresh ESP buffer and incubated at 55 °C for another hour. DNA was purified using phenol:chloroform:isoamyl alcohol (24:24:1) and recovered by precipitation with isopropanol. Cells collected on the 0.1-μm filter were resuspended in 100 μLof Tris-EDTA (pH 8.0) and 100 mg/mL lysozyme before incubating at 37 °C for 30 min. Then, 3.0 mL of a solution containing 5 M guanidinium thiocyanate, 100 mM EDTA (pH 8.0), and 0.5% (vol/vol) sarkosyl was added. The solution was mixed gently for 15 min before being cooled on ice for 10 min. After cooling, an equal volume of cold 7.5 M ammonium acetate was added, and the solution was mixed gently and cooled on ice. Purification and precipitation of DNA were performed with chloroform:isoamyl alcohol (24:1) and isopropanol. Genome Sequencing. Acompletelysequencedandclosedgenome of N. maritimus was obtained through collaboration with the Joint Genome Institute. Whole-genome shotgun sequencing of 3-, 8-, and 40-kb DNA libraries produced at least 8× coverage of the entire genome. Specifics of clone library generation, sequencing, and assembly strategies may be found at the DOE JGI website (www.jgi.doe.gov/sequencing/index.html). Genome Sequence Analysis. Autoannotation of the closed genome sequence was performed by both the Computational Biology group at Oak Ridge National Laboratory (http://genome.ornl. gov/microbial/nmar/02jul07/) and the TIGR Autoannotation Service (now hosted by JCVI; details available from http://www. jcvi.org/cms/research/projects/annotation-service/overview/). The genome visualization software Manatee (release 2.4.1; latest version available from http://manatee.sourceforge.net/) was used for manual curation. Analysis of potential transporter genes was performed using the Transporter Automatic Annotation Pipeline (TransAAP) through the TransportDB genomic comparison tool (membranetransport.org). Direct comparisons with the C. symbiosum genome and genome fragments were performed using the Artemis Comparison Tool (3) 1. Könneke M, et al. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546. 2. Stein LY, et al. (2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: Implications for niche adaptation. Environ Microbiol 9: 2993–3007. 3. Carver TJ, et al. (2005) ACT: The Artemis comparison tool. Bioinformatics 21:3422–3423. 4. Bland C, et al. (2007) CRISPR recognition tool (CRT): A tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8:209. 5. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252. with a comparison library generated through WebACT (www. webact.org/WebACT/home). Orthologous genes shared between these two organisms were identified through reciprocal BLAST searches, with an expectation cutoff value of 10 −4 and a minimum of 75% alignable N. maritimus sequence. Comparisons with the Global Ocean Sampling (GOS) and Sargasso Sea metagenomic datasets were performed using several single-copy universal archaeal genes to determine a count of ∼15 archaeal genomes in the GOS dataset. An initial set of candidate N. maritimus-like proteins was found by BLASTP searches with each N. maritimus proteincoding gene, using a cutoff of 100 hits and a maximum expected value of e = 10. This set consisted of 125,326 peptides drawn from 107,223 scaffolds. Neighboring ORFs on any scaffold with two or more hits were added to make a total of 319,585 peptides, amounting to 5.2% of all ORFs in GOS. These sequences were filtered by BLAST alignment to four sequence datasets, containing 24 complete proteomes from diverse euryarchaeota, crenarchaeota, and bacteria. Sequences scoring more highly to N. maritimus and/or C. symbiosum proteins than any other entry in these datasets were retained, giving a filtered dataset of 21,278 ORFs. Coverage of the N. maritimus proteome was measured by bidirectional BLASTP of N. maritimus proteins against the filtered dataset to assign putative orthologs. The average coverage was ∼11×, although some highly conserved genes had a much greater number of hits, probably due to recruitment of nonarchaeal homologs: 48 ORFs had >30 hits, of which most were highly conserved. Searches for CRISPR regions were performed using the Java-based CRISPR recognition tool (CRT) with least stringent settings (4). Maximum-Likelihood and Bayesian Trees of the Archaeal Domain. The trees are based on the concatenation of ribosomal proteins used by Brochier-Armanet et al. (5) but including sequences from N. maritimus and from “Candidatus Korarchaeum cryptofilum” OPF8. Sequences were aligned using MUSCLE (6). Resulting alignments were visually inspected and improved with the MUST software (7). Regions where homology between sites was doubtful were removed from further phylogenetic analyses. A total of 6,142 positions were kept for the phylogenetic analyses. The maximum-likelihood tree was computed with PHYML, using the WAG model corrected by a gamma law to take into account evolutionary rate among site variations (8). The parameter alpha of the gamma distribution as the proportion of invariable sites was estimated from the dataset. The robustness of each branch was estimated by the bootstrap procedure implemented in PHYML. A Bayesian tree analysis on a subset of 29 taxa was performed using MrBayes 3.2 (9) with a mixed model of amino acid substitution and a gamma distribution (eight discrete categories and an estimated proportion of invariant sites) to take into account among-site rate variation. MrBayes was run with four chains for 1 million generations and trees were sampled every 100 generations. To construct the consensus tree, the first 1,500 trees were discarded as ‘‘burn-in.’’ The reduction of the taxonomic sampling was necessary to reduce the computation time. 6. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. 7. Philippe H (1993) MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res 21:5264–5272. 8. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. 9. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. Walker et al. www.pnas.org/cgi/content/short/0913533107 1of5
Page 1 and 2: Nitrosopumilus maritimus genome rev
Page 3 and 4: ammonia oxidation. There are two hy
Page 5: Fig. 3. Comparison of N. maritimus
Page 9 and 10: Fig. S2. Archaeal ammonia monooxyge
Page 11 and 12: A. 0.1 B. 100 90 52 Other Supportin
Page 13 and 14: Supplemental Table 2: Predicted coo
Page 15 and 16: Supplemental Table 3: Gene predicti
Page 17 and 18: Nmar_tR26 1,630,610 1,630,537 ProGG
Page 19 and 20: Supplemental Table 4: Gene predicti
Page 21 and 22: Nmar_0258 CENSYa_1705 82 227,624 22
Page 29 and 30: Nmar_1303 CENSYa_0131 86 1,193,261
Page 35 and 36: Molybdopterin-guanine dinucleotide
Page 37 and 38: Nmar0935 DeepAntEC39 f 815,847 816,
Page 39 and 40: Nmar0101 EQ085329 r 91,543 93,711 A
Page 41 and 42: Nmar0436 EQ085799 f 386,930 387,319
Page 43 and 44: Nmar0982 EP710054 r 859,116 859,526
Page 45 and 46: Nmar1297 EQ086682 f 1,187,165 1,188

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