Abstract
The South African legumes Lotononis bainesii, L. listii and L. solitudinis are specifically nodulated by highly effective, pink-pigmented bacteria that are most closely related to Methylobacterium nodulans on the basis of 16S rRNA gene homology. Methylobacterium spp. are characterized by their ability to utilize methanol and other C1 compounds, but 11 Lotononis isolates neither grew on methanol as a sole carbon source nor were able to metabolize it. No product was obtained for PCR amplification of mxaF, the gene encoding the large subunit of methanol dehydrogenase. Searches for methylotrophy genes in the sequenced genome of Methylobacterium sp. 4-46, isolated from L. bainesii, indicate that the inability to utilize methanol may be due to the absence of the mxa operon. While methylotrophy appears to contribute to the effectiveness of the Crotalaria/M. nodulans symbiosis, our results indicate that the ability to utilize methanol is not a factor in the Lotononis/Methylobacterium symbiosis.
Similar content being viewed by others
References
Abanda-Nkpwatt D, Musch M, Tschiersch J, Boettner M, Schwab W (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57:4025–4032. doi:10.1093/jxb/erl173
Amaratunga K, Goodwin PM, O’Connor CD, Anthony C (1997) The methanol oxidation genes mxaFJGIR(S)ACKLD in Methylobacterium extorquens. FEMS Microbiol Lett 146:31–38. doi:10.1111/j.1574-6968.1997.tb10167.x
Anthony C (1996) Quinoprotein-catalysed reactions. Biochem J 320:697–711
Basile DV, Basile MR, Li QY, Corpe WA (1985) Vitamin B12-stimulated growth and development of Jungermannia leiantha Grolle and Gymnocolea inflata (Huds.) Dum. (Hepaticae). Bryologist 88:77–81
Belgian Co-ordinated Collection of Microorganisms/Laboratorium voor Microbiologie (1998) Bacterial culture media catalogue. Universiteit Gent, Gent
Chistoserdova L, Chen SW, Lapidus A, Lidstrom ME (2003) Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J Bacteriol 185:2980–2987. doi:10.1128/JB.185.10.2980-2987.2003
Corpe WA, Rheem S (1989) Ecology of the methylotrophic bacteria on living leaf surfaces. FEMS Microbiol Ecol 62:243–249. doi:10.1111/j.1574-6968.1989.tb03698.x
Gallego V, Garcia MT, Ventosa A (2006) Methylobacterium adhaesivum sp. nov., a methylotrophic bacterium isolated from drinking water. Int J Syst Evol Microbiol 56:339–342. doi:10.1099/ijs.0.63966-0
Goodwin PM, Anthony C (1998) The biochemistry, physiology and genetics of PQQ and PQQ-containing enzymes. Adv Microb Physiol 40:1–80
Green PN (1992) The Genus Methylobacterium. In: Balows A, Trüper HG, Dworkin M, Harder W, Schliefer KH (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. Springer, New York, pp 2342–2349
Holland MA, Polacco JC (1994) PPFMs and other covert contaminants—is there more to plant physiology than just plant. Annu Rev Plant Physiol Plant Mol Biol 45:197–209. doi:10.1146/annurev.pp.45.060194.001213
Howieson JG, Ewing MA (1986) Acid tolerance in the Rhizobium meliloti-Medicago symbiosis. Aust J Agric Res 37:153–155. doi:10.1071/AR9860055
Howieson JG, Ewing MA, D’Antuono MF (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105:179–188
Ivanova EG, Doronina NV, Shepelyakovskaya AO, Laman AG, Brovko FA, Trotsenko YA (2000) Facultative and obligate aerobic methylobacteria synthesize cytokinins. Microbiology 69:646–651. doi:10.1023/A:1026693805653
Jaftha JB, Strijdom BW, Steyn PL (2002) Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Syst Appl Microbiol 25:440–449. doi:10.1078/0723-2020-00124
Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139. doi:10.1099/00207713-32-1-136
Jourand P, Renier A, Rapior S, de Faria SM, Prin Y, Galiana A, Giraud E, Dreyfus B (2005) Role of methylotrophy during symbiosis between Methylobacterium nodulans and Crotalaria podocarpa. Mol Plant Microbe Interact 18:1061–1068. doi:10.1094/MPMI-18-1061
Kato Y, Asahara M, Goto K, Kasai H, Yokota A (2008) Methylobacterium persicinum sp. nov., Methylobacterium komagatae sp. nov., Methylobacterium brachiatum sp. nov., Methylobacterium tardum sp. nov. and Methylobacterium gregans sp. nov., isolated from freshwater. Int J Syst Evol Microbiol 58:1134–1141. doi:10.1099/ijs.0.65583-0
Lidstrom ME (2006) Aerobic methylotrophic prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology and biochemistry. Springer, New York, pp 618–634
Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–78. doi:10.1080/0735268031878372
Madhaiyan M, Poonguzhali S, Senthilkumar M, Seshadri S, Chung HY, Yang JC, Sundaram S, Sa TM (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium spp. Bot Bull Acad Sinica 45:315–324
Marx CJ, Chistoserdova L, Lidstrom ME (2003) Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J Bacteriol 185:7160–7168. doi:10.1128/JB.185.23.7160-7168.2003
Miller JA, Kalyuzhnaya MG, Noyes E, Lara JC, Lidstrom ME, Chistoserdova L (2005) Labrys methylaminiphilus sp. nov., a novel facultatively methylotrophic bacterium from a freshwater lake sediment. Int J Syst Evol Microbiol 55:1247–1253. doi:10.1099/ijs.0.63409-0
McDonald IR, Kenna EM, Murrell JC (1995) Detection of methanotrophic bacteria in environmental samples with the PCR. Appl Environ Microbiol 61:116–121
Nash T (1953) The colorimetric estimation of formaldehyde by means of the Hantsch reaction. Biochem J 55:416–421
Norris DO (1958) A red strain of Rhizobium from Lotononis bainesii Baker. Aust J Agric Res 9:629–632. doi:10.1071/AR9580629
O’Brien JR, Murphy JM (1993) Identification and growth characteristics of pink pigmented oxidative bacteria, Methylobacterium mesophilicum and biovars isolated from chlorinated and raw water supplies. Microbios 73:215–227
O’Hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl Environ Microbiol 55:1870–1876
Obendorf RL, Koch JL, Gorecki RJ, Amable RA, Aveni MT (1990) Methanol accumulation in maturing seeds. J Exp Bot 41:489–495
Omer ZS, Tombolini R, Gerhardson B (2004) Plant colonization by pink-pigmented facultative methylotrophic bacteria (PPFMs). FEMS Microbiol Ecol 47:319–326. doi:10.1016/S0168-6496(04)00003-0
Patt TE, Cole GC, Hanson RS (1976) Methylobacterium, a new genus of facultatively methylotrophic bacteria. Int J Syst Bacteriol 26:226–229. doi:10.1099/00207713-26-2-226
Ryu J, Madhaiyan M, Poonguzhali S, Yim W, Indiragandhi P, Kim K, Anandham R, Yun J, Kim KH, Sa T (2006) Plant growth substances produced by Methylobacterium spp. and their effect on tomato (Lycopersicon esculentum L.) and red pepper (Capsicum annuum L.) growth. J Microbiol Biotechnol 16:1622–1628
Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220. doi:10.1128/JB.183.1.214-220.2001
Sy A, Timmers ACJ, Knief C, Vorholt JA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71:7245–7252. doi:10.1128/AEM.71.11.7245-7252.2005
Trotsenko YA, Ivanova EG, Doronina NV (2001) Aerobic methylotrophic bacteria as phytosymbionts. Microbiology 70:623–632. doi:10.1023/A:1013167612105
Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor JL (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides × nigra DN34). Int J Syst Evol Microbiol 54:1191–1196. doi:10.1099/ijs.0.02796-0
Van Wyk BE (1991) A synopsis of the genus Lotononis (Fabaceae: Crotolarieae). Contributions from the Bolus Herbarium No. 14. Rustica Press, Cape Town
Van Wyk BE, Verdoorn GH (1990) Alkaloids as taxonomic characters in the tribe Crotalarieae (Fabaceae). Biochem Syst Ecol 18:503–516
Vogel AI (1962) A text-book of quantitative inorganic analysis. Longman Group, London
Wood PJ, Siddiqui IR (1971) Determination of methanol and its application to measurement of pectin ester content and pectin methyl esterase activity. Anal Biochem 39:418–428
Yates RJ, Howieson JG, Reeve WG, Nandasena K, Law IJ, Bräu L, Ardley JK, Nistelberger H, Real D, O’Hara GW (2007) Lotononis angolensis forms nitrogen fixing, lupinoid nodules with phylogenetically unique fast-growing, pink-pigmented bacteria which do not nodulate L. bainesii or L. listii. Soil Biol Biochem 39:1680–1688. doi:10.1016/j.soilbio.2007.01.025
Acknowledgments
J.A. is the recipient of a Murdoch University Research Scholarship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Rights and permissions
About this article
Cite this article
Ardley, J.K., O’Hara, G.W., Reeve, W.G. et al. Root nodule bacteria isolated from South African Lotononis bainesii, L. listii and L. solitudinis are species of Methylobacterium that are unable to utilize methanol. Arch Microbiol 191, 311–318 (2009). https://doi.org/10.1007/s00203-009-0456-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-009-0456-0