Marine Genomics 23 (2015) 23–25
Contents lists available at ScienceDirect
Marine Genomics journal homepage: www.elsevier.com/locate/margen
Genomics/technical resources
Draft genome of Marinomonas sp. BSi20584 from Arctic sea ice Li Liao a, Xi Sun a,b, Yong Yu a, Bo Chen a,⁎ a b
SOA Key Laboratory for Polar Science, Polar Research Institute of China, Shanghai 200136, China College of Bioengineering, East China University of Science and Technology, Shanghai 200237, China
a r t i c l e
i n f o
Article history: Received 15 February 2015 Received in revised form 31 March 2015 Accepted 31 March 2015 Available online 7 April 2015 Keywords: Arctic Sea ice Marinomonas Polar regions Genome
a b s t r a c t Life surviving in extremely cold frozen environments has been largely uninvestigated. Here we described the draft genome of Marinomonas sp. BSi20584, isolated from Arctic sea ice in the Canada Basin. The assembled genome comprised 4.85 Mb, with the G + C content of 42.6%. Single copy of rRNA operon was detected, which may increase fitness in cold and nutrient-limited environment. In addition, BSi20584 may also use universal strategies for cold adaptation as indicated by the genome. Abundant genes responsible for decomposition of aromatic hydrocarbons were detected, which suggested potential biotechnological applications. The first genomic analysis of Marinomonas in Arctic sea ice provided primary genetic information and encouraged further research on comparative genomics and biotechnological applications. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The Arctic is characterized by extremely low temperature, strong solar radiation and being covered by sea ice for most part. The sea ice is a challenging niche for microorganisms, due to its dynamic temperatures from surface to bottom, and high salinity in brine inclusions (Collins et al., 2010). In addition, the frozen environment is of great interest in astrobiology. Bacteria have been detected alive in the high Arctic sea ice (Junge et al., 2004). However, our understanding of microorganisms inhabiting sea ice is still very limited. Although 24 species have been described in the genus Marinomonas (http://www.bacterio.net/-allnamesmr.html), only six genomes are available in the GenBank (Table 1), including complete genomes of M. posidonica IVIA-Po-181 (Lucas-Elío et al., 2012a), M. mediterranea MMB-1 (Lucas-Elío et al., 2012b) and Marinomonas sp. MWYL1 (NC_ 009654), as well as draft genomes of Marinomonas sp. MED121 (NZ_AANE01000000), M. ushuaiensis DSM 15871 (NZ_JAMB00000000) and Marinomonas sp. D104 (Dong et al., 2014). As a widely distributed marine genus, more investigations at genomic level are required to improve our understanding of its ecology, physiology, genetics and potential in biotechnological applications. Psychrotrophic Marinomonas sp. BSi20584 was isolated from the top 10 cm of an ice core sampled from the high Arctic Canada Basin, during the Second Chinese National Arctic Research Expedition in 2003. The strain was deposited in the Marine Culture Collection of China under the accession number MCCC 1C00250. The 16S rRNA gene shared 99.66% identity with the type strain M. polaris CK13T (AJ833000). ⁎ Corresponding author. Tel.: +86 21 50385104; fax: +86 21 58711663. E-mail address: [email protected] (B. Chen).
http://dx.doi.org/10.1016/j.margen.2015.03.013 1874-7787/© 2015 Elsevier B.V. All rights reserved.
Currently, neither genome of this species nor Marinomonas genome from Arctic sea ice was reported. To fill this gap, Marinomonas sp. BSi20584 was chosen for genome sequencing. Genomic DNA was extracted using the Bacterial Genomic DNA Miniprep Kit (BioDev-Tech Co., China). Pair end (2 × 100 bp) sequencing was performed on the Illumina Hiseq 2000 platform. Raw data was filtered and then assembled by using SOAPdenovo v2.04 (Luo et al., 2012). Transfer RNAs and ribosomal RNAs were predicted by using tRNAscan-SE v1.3.1 (Schattner et al., 2005) and Barrnap 0.4.2 (http:// www.vicbioinformatics.com/software.barrnap.shtml), respectively. Genes were predicted by using Glimmer 3.02 (Delcher et al., 2007), and annotated by searching against the NCBI-nr and KEGG databases. Phylogenetic tree was built based on concatenated alignments of potential orthologous protein sequences (Brown et al., 2001; Strous et al., 2006; Wolf et al., 2002). A total of 1765 single-copy genes shared by all the Marinomonas genomes available in the GenBank and the genome of Marinomonas sp. BSi20584 were aligned in ClustalX 2.0 (Larkin et al., 2007) and concatenated to construct a neighbor-joining tree using MEGA5 (Tamura et al., 2011). The assembled genome consisted of 4,848,582 bp (67 scaffolds), with the G + C content of 42.6%, falling in the range of known Marinomonas genomes (Table 1). A total of 60 tRNAs, 3 rRNAs and 4462 genes were predicted in the draft genome (Table 1). The most similar genome of Marinomonas sp. BSi20584 was Marinomonas sp. MWYL1, which was isolated from the root surface of the salt marsh grass Spartina anglica and able to degrade dimethylsulfoniopropionate (DMSP) (Ansede et al., 2001; Howard et al., 2008), as revealed by phylogenetic analysis based on concatenated alignments (Fig. 1). The second closest genome was Marinomonas sp. D104, which was isolated from deep-sea sediment from Makarov Basin, Arctic Ocean and showed
24
L. Liao et al. / Marine Genomics 23 (2015) 23–25
Table 1 Genome features of Marinomonas sp. BSi20584 compared with other six Marinomonas genomes. Strain
Origin
Size (bp)
Contigs
GC (%)
Genes
rRNA genes
tRNA genes
16S rRNA identity1
BSi20584 MWYL1 IVIA-Po-181 MMB-1 MED121 DSM 15871 D104
Arctic sea ice Salt marsh grass rhizosphere Seagrass Mediterranean coast seawater Mediterranean Sea Coastal seawater Marine sediment
4,848,582 5,100,344 3,899,940 4,684,316 5,153,226 3,342,098 3,833,369
73 1 1 1 47 39 62
42.6 42.6 44.3 44.1 40.9 41.1 44.8
4462 4598 3652 4330 4908 3168 3675
3 25 24 21 17 5 4
60 83 80 78 71 58 63
100% 98% 96% 94% 94% 97% 96%
1
Identity compared to 16S rRNA gene of Marinomonas sp. BSi20584.
Fig. 1. Phylogenetic tree of genome-sequenced Marinomonas.
potential abilities in degradation of polycyclic aromatic hydrocarbons (Dong et al., 2014). The genomic analysis showed that Marinomonas sp. BSi20584 had genetic capacity for adaptation to the cold and salty niche in Arctic sea ice. The widely used strategies to cope with low temperature and/or hyper-osmolality such as molecular chaperones, heat/cold shock proteins, DNA repair systems, maintenance of membrane fluidity and accumulation of compatible solutes were also applicable in BSi20584, as indicated by the genome. In addition, BSi20584 also had unique features for adaptation. For example, a novel heat shock protein gene (TY87_15825) shared modest identity with that of Escherichia coli but no similarity with genes from Marinomonas, suggesting horizontal gene transfer. Moreover, there was a distinct bias of rRNA operon numbers between Marinomonas, with around 6 to 8 copies in Marinomonas isolated from temperate or tropical regions (Marinomonas sp. MWYL1, M. posidonica IVIA-Po-181, M. mediterranea MMB-1, and Marinomonas sp. MED121), while only 1 or 2 copies in Marinomonas isolated from sub-Antarctica or the Arctic (Marinomonas sp. D104, M. ushuaiensis DSM15871, and Marinomonas sp. BSi20584). It was reported that rRNA operon copy number might be related to the response rate to resource availability (Klappenbach et al., 2000). Multiple copies of rRNA operon allow microorganisms to respond quickly to fluctuating environmental conditions, while fewer rRNA operons may lead to slow reaction. However, the constitutive expression from multiple rRNA operons is energy-costive, especially for slow-growing bacteria. Therefore, single copy of rRNA operon in BSi20584 is favored for adaptation to slow growth in nutrient-poor Arctic sea ice, which is probably true for the other two psychrotolerant Marinomonas strains. Central metabolism of BSi20584 seems overall to be similar to other Marinomonas, e.g., full glycolysis/gluconeogenesis, citrate cycle and pentose phosphate pathway etc. were present in all Marinomonas. However, metabolic differences were predicted in many other pathways among them. For example, BSi20584 had more genes responsible for degradation of aromatic compounds than the other Marinomonas, providing unique genetic abilities in degradation of benzoate and xylenes in addition to other commonly degraded aromatic hydrocarbons. This genetic ability may be further exploited in biotechnological
applications. Like the two psychrotolerant strains Marinomonas sp. D104 and M. ushuauensus DSM15871, BSi20584 lacked the gene cluster responsible for DMSP degradation, which occurred in the other four strains. Fewer genes encoding transposase and inactivated derivatives (8 genes) were found in the BSi20584 genome, compared with the other Marinomonas (about 12 to 56 genes), which suggested that the BSi20584 genome was probably less dynamic. In summary, we reported the first Marinomonas genome from Arctic sea ice, and provided primary information on its adaptation and metabolism. Further experimental evidences to support the prediction deduced from the genome sequence would provide a better understanding of this psychrotolerant Marinomonas species. 2. Nucleotide sequence accession numbers The whole genome shotgun project has been deposited in DDBJ/ EMBL/GenBank database under the accession number JYBL00000000. Acknowledgments We appreciate the assistance of the Chinese Arctic and Antarctic Administration (CAA) for organization of the Second Chinese National Arctic Research Expedition in 2003. This work was supported by grants from National Natural Science Foundation of China (Grant No. 41406181), Shanghai Natural Science Foundation (Grant No. 13ZR1462700) and Chinese Polar Environment Comprehensive Investigation, Assessment Program (Grant No. CHINARE04-03) and National High-Tech Research and Development Program of China (Grant No. 2012AA092105). References Ansede, J.H., Pellechia, P.J., Yoch, D.C., 2001. Nuclear magnetic resonance analysis of [1-13C]dimethylsulfoniopropionate (DMSP) and [1-13C]acrylate metabolism by a DMSP lyase-producing marine isolate of the alpha-subclass of Proteobacteria. Appl. Environ. Microbiol. 67, 3134–3139. Brown, J.R., Douady, C.J., Italia, M.J., Marshall, W.E., Stanhope, M.J., 2001. Universal trees based on large combined protein sequence data sets. Nat. Genet. 28, 281–285. Collins, R.E., Rocap, G., Deming, J.W., 2010. Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ. Microbiol. 12, 1828–1841.
L. Liao et al. / Marine Genomics 23 (2015) 23–25 Delcher, A.L., Bratke, K.A., Powers, E.C., Salzberg, S.L., 2007. Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatics 23, 673–679. Dong, C., Bai, X., Lai, Q., Xie, Y., Chen, X., Shao, Z., 2014. Draft genome sequence of Marinomonas sp. strain D104, a polycyclic aromatic hydrocarbon-degrading bacterium from the deep-sea sediment of the Arctic Ocean. Genome Announc. 2, 1211–1213. Howard, E.C., Sun, S., Biers, E.J., Moran, M.A., 2008. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ. Microbiol. 10, 2397–2410. Junge, K., Eicken, H., Deming, J.W., 2004. Bacterial activity at −2 to −20 °C in Arctic wintertime sea ice. Appl. Environ. Microbiol. 70, 550–557. Klappenbach, J.A., Dunbar, J.M., Schmidt, T.M., 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66, 1328–1333. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. Lucas-Elío, P., Goodwin, L., Woyke, T., Pitluck, S., Nolan, M., Kyrpides, N.C., Detter, J.C., Copeland, A., Lu, M., Bruce, D., Detter, C., Tapia, R., Han, S., Land, M.L., Ivanova, N., Mikhailova, N., Johnston, A.W.B., Sanchez-Amat, A., 2012a. Complete genome sequence of Marinomonas posidonica type strain (IVIA-Po-181T). Stand. Genomic Sci. 7, 31–43. Lucas-Elío, P., Goodwin, L., Woyke, T., Pitluck, S., Nolan, M., Kyrpides, N.C., Detter, J.C., Copeland, A., Teshima, H., Bruce, D., Detter, C., Tapia, R., Han, S., Land, M.L., Ivanova, N., Mikhailova, N., Johnston, A.W.B., Sanchez-Amat, A., 2012b. Complete genome
25
sequence of the melanogenic marine bacterium Marinomonas mediterranea type strain (MMB-1T). Stand. Genomic Sci. 6, 63–73. Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., Tang, J., Wu, G., Zhang, H., Shi, Y., Liu, Y., Yu, C., Wang, B., Lu, Y., Han, C., Cheung, D.W., Yiu, S.-M., Peng, S., Xiaoqian, Z., Liu, G., Liao, X., Li, Y., Yang, H., Wang, J., Lam, T.-W., Wang, J., 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 18. Schattner, P., Brooks, A.N., Lowe, T.M., 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686–W689. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., Barbe, V., Fonknechten, N., Vallenet, D., Segurens, B., Schenowitz-Truong, C., Médigue, C., Collingro, A., Snel, B., Dutilh, B.E., Op den Camp, H.J.M., van der Drift, C., Cirpus, I., van de Pas-Schoonen, K.T., Harhangi, H.R., van Niftrik, L., Schmid, M., Keltjens, J., van de Vossenberg, J., Kartal, B., Meier, H., Frishman, D., Huynen, M.A., Mewes, H.-W., Weissenbach, J., Jetten, M.S.M., Wagner, M., Le Paslier, D., 2006. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739. Wolf, Y.I., Rogozin, I.B., Grishin, N.V., Koonin, E.V., 2002. Genome trees and the tree of life. Trends Genet. 18, 472–479.
Contents lists available at ScienceDirect
Marine Genomics journal homepage: www.elsevier.com/locate/margen
Genomics/technical resources
Draft genome of Marinomonas sp. BSi20584 from Arctic sea ice Li Liao a, Xi Sun a,b, Yong Yu a, Bo Chen a,⁎ a b
SOA Key Laboratory for Polar Science, Polar Research Institute of China, Shanghai 200136, China College of Bioengineering, East China University of Science and Technology, Shanghai 200237, China
a r t i c l e
i n f o
Article history: Received 15 February 2015 Received in revised form 31 March 2015 Accepted 31 March 2015 Available online 7 April 2015 Keywords: Arctic Sea ice Marinomonas Polar regions Genome
a b s t r a c t Life surviving in extremely cold frozen environments has been largely uninvestigated. Here we described the draft genome of Marinomonas sp. BSi20584, isolated from Arctic sea ice in the Canada Basin. The assembled genome comprised 4.85 Mb, with the G + C content of 42.6%. Single copy of rRNA operon was detected, which may increase fitness in cold and nutrient-limited environment. In addition, BSi20584 may also use universal strategies for cold adaptation as indicated by the genome. Abundant genes responsible for decomposition of aromatic hydrocarbons were detected, which suggested potential biotechnological applications. The first genomic analysis of Marinomonas in Arctic sea ice provided primary genetic information and encouraged further research on comparative genomics and biotechnological applications. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The Arctic is characterized by extremely low temperature, strong solar radiation and being covered by sea ice for most part. The sea ice is a challenging niche for microorganisms, due to its dynamic temperatures from surface to bottom, and high salinity in brine inclusions (Collins et al., 2010). In addition, the frozen environment is of great interest in astrobiology. Bacteria have been detected alive in the high Arctic sea ice (Junge et al., 2004). However, our understanding of microorganisms inhabiting sea ice is still very limited. Although 24 species have been described in the genus Marinomonas (http://www.bacterio.net/-allnamesmr.html), only six genomes are available in the GenBank (Table 1), including complete genomes of M. posidonica IVIA-Po-181 (Lucas-Elío et al., 2012a), M. mediterranea MMB-1 (Lucas-Elío et al., 2012b) and Marinomonas sp. MWYL1 (NC_ 009654), as well as draft genomes of Marinomonas sp. MED121 (NZ_AANE01000000), M. ushuaiensis DSM 15871 (NZ_JAMB00000000) and Marinomonas sp. D104 (Dong et al., 2014). As a widely distributed marine genus, more investigations at genomic level are required to improve our understanding of its ecology, physiology, genetics and potential in biotechnological applications. Psychrotrophic Marinomonas sp. BSi20584 was isolated from the top 10 cm of an ice core sampled from the high Arctic Canada Basin, during the Second Chinese National Arctic Research Expedition in 2003. The strain was deposited in the Marine Culture Collection of China under the accession number MCCC 1C00250. The 16S rRNA gene shared 99.66% identity with the type strain M. polaris CK13T (AJ833000). ⁎ Corresponding author. Tel.: +86 21 50385104; fax: +86 21 58711663. E-mail address: [email protected] (B. Chen).
http://dx.doi.org/10.1016/j.margen.2015.03.013 1874-7787/© 2015 Elsevier B.V. All rights reserved.
Currently, neither genome of this species nor Marinomonas genome from Arctic sea ice was reported. To fill this gap, Marinomonas sp. BSi20584 was chosen for genome sequencing. Genomic DNA was extracted using the Bacterial Genomic DNA Miniprep Kit (BioDev-Tech Co., China). Pair end (2 × 100 bp) sequencing was performed on the Illumina Hiseq 2000 platform. Raw data was filtered and then assembled by using SOAPdenovo v2.04 (Luo et al., 2012). Transfer RNAs and ribosomal RNAs were predicted by using tRNAscan-SE v1.3.1 (Schattner et al., 2005) and Barrnap 0.4.2 (http:// www.vicbioinformatics.com/software.barrnap.shtml), respectively. Genes were predicted by using Glimmer 3.02 (Delcher et al., 2007), and annotated by searching against the NCBI-nr and KEGG databases. Phylogenetic tree was built based on concatenated alignments of potential orthologous protein sequences (Brown et al., 2001; Strous et al., 2006; Wolf et al., 2002). A total of 1765 single-copy genes shared by all the Marinomonas genomes available in the GenBank and the genome of Marinomonas sp. BSi20584 were aligned in ClustalX 2.0 (Larkin et al., 2007) and concatenated to construct a neighbor-joining tree using MEGA5 (Tamura et al., 2011). The assembled genome consisted of 4,848,582 bp (67 scaffolds), with the G + C content of 42.6%, falling in the range of known Marinomonas genomes (Table 1). A total of 60 tRNAs, 3 rRNAs and 4462 genes were predicted in the draft genome (Table 1). The most similar genome of Marinomonas sp. BSi20584 was Marinomonas sp. MWYL1, which was isolated from the root surface of the salt marsh grass Spartina anglica and able to degrade dimethylsulfoniopropionate (DMSP) (Ansede et al., 2001; Howard et al., 2008), as revealed by phylogenetic analysis based on concatenated alignments (Fig. 1). The second closest genome was Marinomonas sp. D104, which was isolated from deep-sea sediment from Makarov Basin, Arctic Ocean and showed
24
L. Liao et al. / Marine Genomics 23 (2015) 23–25
Table 1 Genome features of Marinomonas sp. BSi20584 compared with other six Marinomonas genomes. Strain
Origin
Size (bp)
Contigs
GC (%)
Genes
rRNA genes
tRNA genes
16S rRNA identity1
BSi20584 MWYL1 IVIA-Po-181 MMB-1 MED121 DSM 15871 D104
Arctic sea ice Salt marsh grass rhizosphere Seagrass Mediterranean coast seawater Mediterranean Sea Coastal seawater Marine sediment
4,848,582 5,100,344 3,899,940 4,684,316 5,153,226 3,342,098 3,833,369
73 1 1 1 47 39 62
42.6 42.6 44.3 44.1 40.9 41.1 44.8
4462 4598 3652 4330 4908 3168 3675
3 25 24 21 17 5 4
60 83 80 78 71 58 63
100% 98% 96% 94% 94% 97% 96%
1
Identity compared to 16S rRNA gene of Marinomonas sp. BSi20584.
Fig. 1. Phylogenetic tree of genome-sequenced Marinomonas.
potential abilities in degradation of polycyclic aromatic hydrocarbons (Dong et al., 2014). The genomic analysis showed that Marinomonas sp. BSi20584 had genetic capacity for adaptation to the cold and salty niche in Arctic sea ice. The widely used strategies to cope with low temperature and/or hyper-osmolality such as molecular chaperones, heat/cold shock proteins, DNA repair systems, maintenance of membrane fluidity and accumulation of compatible solutes were also applicable in BSi20584, as indicated by the genome. In addition, BSi20584 also had unique features for adaptation. For example, a novel heat shock protein gene (TY87_15825) shared modest identity with that of Escherichia coli but no similarity with genes from Marinomonas, suggesting horizontal gene transfer. Moreover, there was a distinct bias of rRNA operon numbers between Marinomonas, with around 6 to 8 copies in Marinomonas isolated from temperate or tropical regions (Marinomonas sp. MWYL1, M. posidonica IVIA-Po-181, M. mediterranea MMB-1, and Marinomonas sp. MED121), while only 1 or 2 copies in Marinomonas isolated from sub-Antarctica or the Arctic (Marinomonas sp. D104, M. ushuaiensis DSM15871, and Marinomonas sp. BSi20584). It was reported that rRNA operon copy number might be related to the response rate to resource availability (Klappenbach et al., 2000). Multiple copies of rRNA operon allow microorganisms to respond quickly to fluctuating environmental conditions, while fewer rRNA operons may lead to slow reaction. However, the constitutive expression from multiple rRNA operons is energy-costive, especially for slow-growing bacteria. Therefore, single copy of rRNA operon in BSi20584 is favored for adaptation to slow growth in nutrient-poor Arctic sea ice, which is probably true for the other two psychrotolerant Marinomonas strains. Central metabolism of BSi20584 seems overall to be similar to other Marinomonas, e.g., full glycolysis/gluconeogenesis, citrate cycle and pentose phosphate pathway etc. were present in all Marinomonas. However, metabolic differences were predicted in many other pathways among them. For example, BSi20584 had more genes responsible for degradation of aromatic compounds than the other Marinomonas, providing unique genetic abilities in degradation of benzoate and xylenes in addition to other commonly degraded aromatic hydrocarbons. This genetic ability may be further exploited in biotechnological
applications. Like the two psychrotolerant strains Marinomonas sp. D104 and M. ushuauensus DSM15871, BSi20584 lacked the gene cluster responsible for DMSP degradation, which occurred in the other four strains. Fewer genes encoding transposase and inactivated derivatives (8 genes) were found in the BSi20584 genome, compared with the other Marinomonas (about 12 to 56 genes), which suggested that the BSi20584 genome was probably less dynamic. In summary, we reported the first Marinomonas genome from Arctic sea ice, and provided primary information on its adaptation and metabolism. Further experimental evidences to support the prediction deduced from the genome sequence would provide a better understanding of this psychrotolerant Marinomonas species. 2. Nucleotide sequence accession numbers The whole genome shotgun project has been deposited in DDBJ/ EMBL/GenBank database under the accession number JYBL00000000. Acknowledgments We appreciate the assistance of the Chinese Arctic and Antarctic Administration (CAA) for organization of the Second Chinese National Arctic Research Expedition in 2003. This work was supported by grants from National Natural Science Foundation of China (Grant No. 41406181), Shanghai Natural Science Foundation (Grant No. 13ZR1462700) and Chinese Polar Environment Comprehensive Investigation, Assessment Program (Grant No. CHINARE04-03) and National High-Tech Research and Development Program of China (Grant No. 2012AA092105). References Ansede, J.H., Pellechia, P.J., Yoch, D.C., 2001. Nuclear magnetic resonance analysis of [1-13C]dimethylsulfoniopropionate (DMSP) and [1-13C]acrylate metabolism by a DMSP lyase-producing marine isolate of the alpha-subclass of Proteobacteria. Appl. Environ. Microbiol. 67, 3134–3139. Brown, J.R., Douady, C.J., Italia, M.J., Marshall, W.E., Stanhope, M.J., 2001. Universal trees based on large combined protein sequence data sets. Nat. Genet. 28, 281–285. Collins, R.E., Rocap, G., Deming, J.W., 2010. Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ. Microbiol. 12, 1828–1841.
L. Liao et al. / Marine Genomics 23 (2015) 23–25 Delcher, A.L., Bratke, K.A., Powers, E.C., Salzberg, S.L., 2007. Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatics 23, 673–679. Dong, C., Bai, X., Lai, Q., Xie, Y., Chen, X., Shao, Z., 2014. Draft genome sequence of Marinomonas sp. strain D104, a polycyclic aromatic hydrocarbon-degrading bacterium from the deep-sea sediment of the Arctic Ocean. Genome Announc. 2, 1211–1213. Howard, E.C., Sun, S., Biers, E.J., Moran, M.A., 2008. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ. Microbiol. 10, 2397–2410. Junge, K., Eicken, H., Deming, J.W., 2004. Bacterial activity at −2 to −20 °C in Arctic wintertime sea ice. Appl. Environ. Microbiol. 70, 550–557. Klappenbach, J.A., Dunbar, J.M., Schmidt, T.M., 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66, 1328–1333. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. Lucas-Elío, P., Goodwin, L., Woyke, T., Pitluck, S., Nolan, M., Kyrpides, N.C., Detter, J.C., Copeland, A., Lu, M., Bruce, D., Detter, C., Tapia, R., Han, S., Land, M.L., Ivanova, N., Mikhailova, N., Johnston, A.W.B., Sanchez-Amat, A., 2012a. Complete genome sequence of Marinomonas posidonica type strain (IVIA-Po-181T). Stand. Genomic Sci. 7, 31–43. Lucas-Elío, P., Goodwin, L., Woyke, T., Pitluck, S., Nolan, M., Kyrpides, N.C., Detter, J.C., Copeland, A., Teshima, H., Bruce, D., Detter, C., Tapia, R., Han, S., Land, M.L., Ivanova, N., Mikhailova, N., Johnston, A.W.B., Sanchez-Amat, A., 2012b. Complete genome
25
sequence of the melanogenic marine bacterium Marinomonas mediterranea type strain (MMB-1T). Stand. Genomic Sci. 6, 63–73. Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., Tang, J., Wu, G., Zhang, H., Shi, Y., Liu, Y., Yu, C., Wang, B., Lu, Y., Han, C., Cheung, D.W., Yiu, S.-M., Peng, S., Xiaoqian, Z., Liu, G., Liao, X., Li, Y., Yang, H., Wang, J., Lam, T.-W., Wang, J., 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 18. Schattner, P., Brooks, A.N., Lowe, T.M., 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686–W689. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., Barbe, V., Fonknechten, N., Vallenet, D., Segurens, B., Schenowitz-Truong, C., Médigue, C., Collingro, A., Snel, B., Dutilh, B.E., Op den Camp, H.J.M., van der Drift, C., Cirpus, I., van de Pas-Schoonen, K.T., Harhangi, H.R., van Niftrik, L., Schmid, M., Keltjens, J., van de Vossenberg, J., Kartal, B., Meier, H., Frishman, D., Huynen, M.A., Mewes, H.-W., Weissenbach, J., Jetten, M.S.M., Wagner, M., Le Paslier, D., 2006. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739. Wolf, Y.I., Rogozin, I.B., Grishin, N.V., Koonin, E.V., 2002. Genome trees and the tree of life. Trends Genet. 18, 472–479.
