Genome Sequence of the Halotolerant Marine Bacterium Myxococcus ...

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Jun 10, 2011 - The whole genome of M. fulvus HW-1 will enable us to further ... .centerforgenomicsciences.org/) & Beijing Genomics Institute at Shen-.
JOURNAL OF BACTERIOLOGY, Sept. 2011, p. 5015–5016 0021-9193/11/$12.00 doi:10.1128/JB.05516-11 Copyright © 2011, American Society for Microbiology. All Rights Reserved.

Vol. 193, No. 18

Genome Sequence of the Halotolerant Marine Bacterium Myxococcus fulvus HW-1 Zhi-Feng Li,§ Xia Li,§ Hong Liu, Xin Liu, Kui Han, Zhi-Hong Wu, Wei Hu, Fei-fei Li, and Yue-Zhong Li* State Key Laboratory of Microbial Technology, College of Life Science, Shandong University, Jinan 250100, China Received 10 June 2011/Accepted 29 June 2011

Myxococcus fulvus HW-1 (ATCC BAA-855) is a halotolerant marine myxobacterium. This strain exhibits complex social behaviors in the presence of low concentrations of seawater but adopts an asocial living pattern under oceanic conditions. The whole genome of M. fulvus HW-1 will enable us to further investigate the details of its evolution.

M. fulvus HW-1 contains a single circular chromosome of 9,003,593 bp, and the overall GC content is 70.6%. The whole sequence contains 7,361 putative genes, accounting for 85.5% of the genome length. Genes are evenly distributed between the forward (48.8%) and reverse (51.2%) strands. Three rRNA operons, 67 tRNAs, and 7,285 predicted protein-coding sequences (CDSs) were identified in the chromosome. The average length of the CDSs is 1,054 bp, and 63.9% of the CDSs encode proteins whose functions are unknown. A total of 1,081 tandem repeats with a mean copy number of 3.3 were detected by Trf (2). IslandViewer (8) identified 9 genomic islands in the genome. Compared to DK 1622, a global synteny with two large inversions is apparent. The overall average identity of the CDSs is 75.17% between the two genomes. Deep comparative genome analysis is under way. Sequencing of this model halotolerant Myxococcus enables us get a full picture of the evolutionary trail recorded in the genome and further opens the way to understanding the molecular details of their two living patterns and oceanic adaption evolution mechanisms. Nucleotide sequence accession number. The whole-genome sequence was deposited in GenBank under accession number CP002830.

Myxobacteria are Gram-negative single-celled prokaryotes with complex social behaviors (14). Myxobacterial strains are commonly isolated from various terrestrial habitats and are thus regarded as soil-dwelling bacteria (3, 12), which are normally unable to grow with more than 1.0% salt concentration (13). However, some marine halophilic (4, 6, 7) and halotolerant (9) myxobacteria have recently been isolated. While the halophiles are phylogenetically distinct from soil-dwelling myxobacteria, the halotolerants are more closely related to their terrestrial relatives. The halotolerant myxobacteria exhibit complex social living patterns in the presence of low concentrations of saltwater, such as developing fruiting bodies and myxospores, in response to starvation on solid surfaces, similar to those exhibited by soil-dwelling myxobacteria, but they adopt a rather simple living pattern under oceanic conditions, for example, developing myxospores directly from vegetative cells without the formation of fruiting bodies (18). Further studies revealed that halotolerant strains enhance their S motility in high seawater concentrations (16), and salt tolerance is often closely associated with their social behaviors (10, 17). Even more, some horizontally transferred genes confer some advantages for their adaption to life in the ocean (11). Myxococcus fulvus HW-1 (ATCC BAA-855) is a typical halotolerant strain, isolated from a coastal seawater sample (9). The strain is able to grow in medium containing a wide range of seawater concentrations, from 0% to 130% (corresponding salinity concentrations are 0% to 4.7%) (18). The whole genome of M. fulvus HW-1 was sequenced. The sequence data were obtained by a combination of the 454 method, with 23⫻ coverage, and the Illumina method, with 5 paired-end libraries over 100 coverage depths. The Sanger method was employed for closing and validation of the complete genome. The genome of M. xanthus DK 1622 (5) was used as a reference. Genome annotation was performed using the RAST annotation server (1), the BASys bacterial annotation system (15), and NCBI PGAAP servers.

This work was financially supported by the Chinese National Science Foundation for Distinguished Young Scholars (no. 30825001) and the Chinese Natural Science Foundation (no. 30900027&30971572). We thank the Center for Genomic Sciences (CGS) (http://www .centerforgenomicsciences.org/) & Beijing Genomics Institute at Shenzhen (http://www.genomics.cn/index.php) for genome sequencing and assembling. We thank the RAST, BASys, and PGAAP annotation servers. REFERENCES 1. Aziz, R. K., et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. 2. Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573–580. 3. Dawid, W. 2000. Biology and global distribution of myxobacteria in soils. FEMS Microbiol. Rev. 24:403–427. 4. Fudou, R., Y. Jojima, T. Iizuka, and S. Yamanaka. 2002. Haliangium ochraceum gen. nov., sp. nov. and Haliangium tepidum sp. nov.: novel moderately halophilic myxobacteria isolated from coastal saline environments. J. Gen. Appl. Microbiol. 48:109–116. 5. Goldman, B. S., et al. 2006. Evolution of sensory complexity recorded in a myxobacterial genome. Proc. Natl. Acad. Sci. U. S. A. 103:15200–15205. 6. Iizuka, T., et al. 2003. Enhygromyxa salina gen. nov., sp. nov., a slightly

* Corresponding author. Mailing address: State Key Laboratory of Microbial Technology, College of Life Science, Shandong University, Jinan 250100, China. Phone and fax: 86-531-88564288. E-mail: lilab @sdu.edu.cn. § Zhi-Feng Li and Xia Li contributed equally to this work. 5015

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9. 10.

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halophilic myxobacterium isolated from the coastal areas of Japan. Syst. Appl. Microbiol. 26:189–196. Iizuka, T., Y. Jojima, R. Fudou, and S. Yamanaka. 1998. Isolation of myxobacteria from the marine environment. FEMS Microbiol. Lett. 169:317–322. Langille, M. G., and F. S. Brinkman. 2009. IslandViewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics 25:664–665. Li, Y. Z., et al. 2002. A simple method to isolate salt-tolerant myxobacteria from marine samples. J. Microbiol. Methods 50:205–209. Pan, H. W., et al. 2009. Seawater-regulated genes for two-component systems and outer membrane proteins in myxococcus. J. Bacteriol. 191:2102– 2111. Pan, H. W., et al. 2010. Hdsp, a horizontally transferred gene required for social behavior and halotolerance in salt-tolerant Myxococcus fulvus HW-1. ISME J. 4:1282–1289.

J. BACTERIOL. 12. Reichenbach, H. 1999. The ecology of myxobacteria. Environ. Microbiol. 1:15–21. 13. Reichenbach, H., and M. Dworkin. 1992. The myxobacteria., p. 3416–3487. In K. H. Tru ¨per, H. G., Dworkin, M., Harder, W., Schleifer (ed.), The Prokaryotes, 2 ed. Springer, Berlin. 14. Shimkets, L. J. 1990. Social and developmental biology of myxobacteria. Microbiol. Rev. 54:473–501. 15. Van, D. G., et al. 2005. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res. 33:W455–W459. 16. Wang, B., et al. 2007. Adaptation of salt-tolerant Myxococcus strains and their motility systems to the ocean conditions. Microb. Ecol. 54:43–51. 17. Zhang, C. Y., et al. 2007. New locus important for Myxococcus social motility and development. J. Bacteriol. 189:7937–7941. 18. Zhang, Y. Q., et al. 2005. Characteristics and living patterns of marine myxobacterial isolates. Appl. Environ. Microbiol. 71:3331–3336.