A commensal symbiotic interrelationship for the growth of Symbiobacterium toebii with its partner bacterium, Geobacillus toebii

BMC Research Notes

Moon-Hee Sung³  Seiki Kuramitsu²  Ryoji Masui²  Joong-Jae Kim⁴  Kwang Kim¹ 

[1] Department of Biological Sciences, Graduate School of Science, Osaka University, Osaka 560-0043, Japan;RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, Hyogo 679-5148, Japan;Department of Advanced Fermentation Fusion Science and Technology, Kookmin University, Seoul 136-702, Korea;Department of Biological Sciences, University of Calgary, Calgary, Alberta, T2N 1N4, Canada

关键词: Commensalism;    Growth-supporting factor;    Bacterial symbiosis;    Geobacillus toebii;    Symbiobacterium toebii;   

Others  :  1167043
DOI  :  10.1186/1756-0500-4-437

 received in 2011-05-22, accepted in 2011-10-24,  发布年份 2011

【 摘 要 】

Background

Symbiobacterium toebii is a commensal symbiotic thermophile that absolutely requires its partner bacterium Geobacillus toebii for growth. Despite development of an independent cultivation method using cell-free extracts, the growth of Symbiobacterium remains unknown due to our poor understanding of the symbiotic relationship with its partner bacterium. Here, we investigated the interrelationship between these two bacteria for growth of S. toebii using different cell-free extracts of G. toebii.

Results

Symbiobacterium toebii growth-supporting factors were constitutively produced through almost all growth phases and under different oxygen tensions in G. toebii, indicating that the factor may be essential components for growth of G. toebii as well as S. toebii. The growing conditions of G. toebii under different oxygen tension dramatically affected to the initial growth of S. toebii and the retarded lag phase was completely shortened by reducing agent, L-cysteine indicating an evidence of commensal interaction of microaerobic and anaerobic bacterium S. toebii with a facultative aerobic bacterium G. toebii. In addition, the growth curve of S. toebii showed a dependency on the protein concentration of cell-free extracts of G. toebii, demonstrating that the G. toebii-derived factors have nutrient-like characters but not quorum-sensing characters.

Conclusions

Not only the consistent existence of the factor in G. toebii during all growth stages and under different oxygen tensions but also the concentration dependency of the factor for proliferation and optimal growth of S. toebii, suggests that an important biosynthetic machinery lacks in S. toebii during evolution. The commensal symbiotic bacterium, S. toebii uptakes certain ubiquitous and essential compound for its growth from environment or neighboring bacteria that shares the equivalent compounds. Moreover, G. toebii grown under aerobic condition shortened the lag phase of S. toebii under anaerobic and microaerobic conditions, suggests a possible commensal interaction that G. toebii scavengers ROS/RNS species and helps the initial growth of S. toebii.

【 授权许可】

   
2011 Kuramitsu et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Hugenholtz P, Goebel BM, Pace NR: Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998, 180(18):4765-4774.
• [2]Pace NR: A molecular view of microbial diversity and the biosphere. Science 1997, 276(5313):734-740.
• [3]Amann RI, Ludwig W, Schleifer KH: Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995, 59(1):143-169.
• [4]Lee N, Nielsen PH, Andreasen KH, Juretschko S, Nielsen JL, Schleifer KH, Wagner M: Combination of fluorescent in situ hybridization and microautoradiography-a new tool for structure-function analyses in microbial ecology. Appl Environ Microbiol 1999, 65(3):1289-1297.
• [5]Nielsen JL, Christensen D, Kloppenborg M, Nielsen PH: Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ Microbiol 2003, 5(3):202-211.
• [6]Friedrich MW: Stable-isotope probing of DNA: insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. Curr Opin Biotechnol 2006, 17(1):59-66.
• [7]Whiteley AS, Manefield M, Lueders T: Unlocking the 'microbial black box' using RNA-based stable isotope probing technologies. Curr Opin Biotechnol 2006, 17(1):67-71.
• [8]Adamczyk J, Hesselsoe M, Iversen N, Horn M, Lehner A, Nielsen PH, Schloter M, Roslev P, Wagner M: The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function. Appl Environ Microbiol 2003, 69(11):6875-6887.
• [9]Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H: Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000, 407(6800):81-86.
• [10]Tamas I, Klasson LM, Sandstrom JP, Andersson SG: Mutualists and parasites: how to paint yourself into a (metabolic) corner. FEBS Lett 2001, 498(2-3):135-139.
• [11]Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI: A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003, 299(5615):2074-2076.
• [12]Vallesi A, Giuli G, Bradshaw RA, Luporini P: Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 1995, 376(6540):522-524.
• [13]Kaeberlein T, Lewis K, Epstein SS: Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment. Science 2002, 296(5570):1127-1129.
• [14]Rhee SK, Lee SG, Hong SP, Choi YH, Park JH, Kim CJ, Sung MH: A novel microbial interaction: obligate commensalism between a new gram-negative thermophile and a thermophilic Bacillus strain. Extremophiles 2000, 4(3):131-136.
• [15]Rhee SK, Jeon CO, Bae JW, Kim K, Song JJ, Kim JJ, Lee SG, Kim HI, Hong SP, Choi YH, et al.: Characterization of Symbiobacterium toebii, an obligate commensal thermophile isolated from compost. Extremophiles 2002, 6(1):57-64.
• [16]Rhee SK, Hong SP, Bae JW, Jeon CO, Lee SG, Song JJ, Poo H, Sung MH: Estimation of distribution of a commensal thermophile in soil by competitive quantitative PCR and terminal restriction fragment length polymorphism analysis. Journal of Microbiology and Biotechnology 2001, 11(6):940-945.
• [17]Bae JW, Kim JJ, Jeon CO, Kim K, Song JJ, Lee SG, Poo H, Jung CM, Park YH, Sung MH: Application of denaturing gradient gel electrophoresis to estimate the diversity of commensal thermophiles. Journal of Microbiology and Biotechnology 2003, 13(6):1008-1012.
• [18]Bae JW, Rhee SK, Park JR, Kim BC, Park YH: Isolation of uncultivated anaerobic thermophiles from compost by supplementing cell extract of Geobacillus toebii in enrichment culture medium. Extremophiles 2005.
• [19]Ueda K, Ohno M, Yamamoto K, Nara H, Mori Y, Shimada M, Hayashi M, Oida H, Terashima Y, Nagata M, et al.: Distribution and diversity of symbiotic thermophiles, Symbiobacterium thermophilum and related bacteria, in natural environments. Appl Environ Microbiol 2001, 67(9):3779-3784.
• [20]Kim JJ, Masui R, Kuramitsu S, Seo JH, Kim K, Sung MH: Characterization of growth-supporting factors produced by Geobacillus toebii for the commensal thermophile Symbiobacterium toebii. J Microbiol Biotechnol 2008, 18(3):490-496.
• [21]Sung MH, Bae JW, Kim JJ, Kim K, Song JJ, Rhee SK, Jeon CO, Choi YH, Hong SP, Lee SG, et al.: Symbiobacterium toebii sp. nov., Commensal Thermophile Isolated from Korean Compost. Journal of Microbiology and Biotechnology 2003, 13(6):1013-1017.
• [22]Sung MH, Kim H, Bae JW, Rhee SK, Jeon CO, Kim K, Kim JJ, Hong SP, Lee SG, Yoon JH, et al.: Geobacillus toebii sp. nov., a novel thermophilic bacterium isolated from hay compost. Int J Syst Evol Microbiol 2002, 52(Pt 6):2251-2255.
• [23]Jean D, Briolat V, Reysset G: Oxidative stress response in Clostridium perfringens. Microbiology 2004, 150(Pt 6):1649-1659.
• [24]Fareleira P, Santos BS, Antonio C, Moradas-Ferreira P, LeGall J, Xavier AV, Santos H: Response of a strict anaerobe to oxygen: survival strategies in Desulfovibrio gigas. Microbiology 2003, 149(Pt 6):1513-1522.
• [25]Levett PN: Anaerobic Microbiology; A Practical Approach. In Anaerobic culture methods. Volume 1. 1st edition. Edited by Willis AT. Oxford New York Tokyo: Oxford University Press; 1991.
• [26]Takami H, Takaki Y, Chee GJ, Nishi S, Shimamura S, Suzuki H, Matsui S, Uchiyama I: Thermoadaptation trait revealed by the genome sequence of thermophilic Geobacillus kaustophilus. Nucleic Acids Res 2004, 32(21):6292-6303.
• [27]Ji G, Pei W, Zhang L, Qiu R, Lin J, Benito Y, Lina G, Novick RP: Staphylococcus intermedius produces a functional agr autoinducing peptide containing a cyclic lactone. J Bacteriol 2005, 187(9):3139-3150.
• [28]Kleerebezem M, Quadri LE, Kuipers OP, de Vos WM: Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 1997, 24(5):895-904.
• [29]Hastings JW, Greenberg EP: Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. J Bacteriol 1999, 181(9):2667-2668.
• [30]Ueda K, Beppu T: Lessons from studies of Symbiobacterium thermophilum, a unique syntrophic bacterium. Biosci Biotechnol Biochem 2007, 71(5):1115-1121.
• [31]Bradford M: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 1976, 72:248-254.
• [32]Beers RF Jr, Sizer IW: A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 1952, 195(1):133-140.