Abstract
Nineteen fungal strains having an ability to oxidize elemental sulfur in mineral salts medium were isolated from deteriorated sandstones of Angkor monuments. These fungi formed clearing zone on agar medium supplemented with powder sulfur due to the dissolution of sulfur. Representative of the isolates, strain THIF01, was identified as Fusarium solani on the basis of morphological characteristics and phylogenetic analyses. PCR amplification targeting 16S rRNA gene and analyses of full 16S rRNA gene sequence indicated strain THIF01 harbors an endobacterium Bradyrhizobium sp.; however, involvement of the bacterium in the sulfur oxidation is still unclear. Strain THIF01 oxidized elemental sulfur to thiosulfate and then sulfate. Germination of the spores of strain THIF01 was observed in a liquid medium containing mineral salts supplemented with elemental sulfur (rate of germinated spores against total spores was 60.2%), and the culture pH decreased from pH 4.8 to 4.0. On the contrary, neither germination (rate of germinated spores against total spores was 1.0%) nor pH decrease was observed without the supplement of elemental sulfur. Strain THIF01 could also degrade 30 ppmv and ambient level (approximate 500 pptv) of carbonyl sulfide.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Bandy AR, Thornton DC, Scott DL, Lalevic M, Lewin EE, Driedger AR III (1992) A time series for carbonyl sulfide in the northern hemisphere. J Atmos Chem 14:527–534
Bertaux J, Schmid M, Prevost-Boure NC, Churin JL, Hartmann A, Garbaye J, Frey-Klett P (2003) In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Appl Environ Microbiol 69:4243–4248
Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010
Bianciotto V, Lumini E, Lanfranco L, Minerdi D, Bonfante P, Perotto S (2000) Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl Environ Microbiol 66:4503–4509
Burford EP, Fomina M, Gadd GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67:1127–1155
Chin M, Davis DD (1995) A reanalysis of carbonyl sulfide as a source of stratospheric background sulfur aerosol. J Geophys Res 100:8993–9005
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gómez-Alarcón G, Muñoz ML, Flores M (1994) Excretion of organic acids by fungal strains isolated from decayed sandstone. Int Biodeterior Biodegrad 34:169–180
Gorbushina AA, Krumbein WE, Hamman CH, Panina L, Soukharjevski S, Wollenzien U (1993) Role of black fungi in color change and biodeterioration of antique marbles. Geomicrobiol J 11:205–221
Grayston SJ, Nevell W, Wainwright M (1986) Sulphur oxidation by fungi. Trans Br Mycol Soc 87:193–198
Gu JD, Ford TE, Berke NS, Mitchell R (1998) Biodeterioration of concrete by the fungus Fusarium. Int Biodeterior Biodegrad 41:101–109
Gu JD (2009) Corrosion, Microbial. In: Schaechter M (ed) Encyclopedia of Microbiology, 3rd edn. Elsevier, UK
Hosono T, Uchida E, Suda C, Ueno A, Nakagawa T (2006) Salt weathering of sandstone at the Angkor monuments, Cambodia: identification of the origins of salts using sulfur and strontium isotopes. J Archaeol Sci 33:1541–1551
Kato H, Saito M, Nagahata Y, Katayama Y (2008) Degradation of ambient carbonyl sulfide by Mycobacterium spp. in soil. Microbiol 154:249–255
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kurek E (1985) Elemental sulphur and thiosulphate oxidation by Rhodotorula sp. Zbl Mikrobiol 140:497–500
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York
Li XS, Arai H, Shimoda I, Kuraishi H, Katayama Y (2008) Enumeration of sulfur-oxidizing microorganisms on deteriorating stone of the Angkor monuments, Cambodia. Microbes Environ 23:293–298
Lim YW, Baik KS, Han SK, Kim SB, Bae KS (2003) Burkholderia sordidicola sp. nov., isolated from the white-rot fungus Phanerochaete sordida. Int J Syst Evol Microbiol 53:1631–1636
Macdonald RM, Chandler MR, Mosse B (1982) The occurrence of bacterium-like organelles in vesicular-arbuscular mycorrhizal fungi. New Phytol 90:659–663
Masuda S, Eda S, Ikeda S, Mitsui H, Minamisawa K (2010) Thiosulfate-dependent chemolithoautotrophic growth of Bradyrhizobium japonicum. Appl Environ Microbiol 76:2402–2409
Mirocha CJ, DeVay JE (1971) Growth of fungi on an inorganic medium. Can J Microbiol 17:1373–1378
Nelson PE, Toussoun TA, Marasas WFO (1983) Fusalium species: an illustrated manual for identification. The Pennsylvania State University Press, University Park, PA
Parker CD (1947) Species of sulphur bacteria associated with the corrosion of concrete. Nature 159:439–440
Parker CD, Prisk J (1953) The oxidation of inorganic compounds of sulphur by various sulphur bacteria. J Gen Microbiol 8:344–364
Parkinson SM, Wainwright M, Killham K (1989) Observations on oligotrophic growth of fungi on silica gel. Mycol Res 93:529–534
Partida-Martinez LP, Groth I, Schmitt I, Richter W, Roth M, Hertweck C (2007) Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus. Int J Syst Evol Microbiol 57:2583–2590
Partida-Martinez LP, Looß CF, Ishida K, Ishida M, Roth M, Buder K, Hertweck C (2007) Rhizonin, the first mycotoxin isolated from the Zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73:793–797
Perrière G, Gouy M (1996) WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
Ruiz-Lozano JM, Bonfante P (1999) Identification of a putative P-transporter operon in the genome of a Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita. J Bacteriol 181:4106–4109
Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—an updated overview. Adv Appl Microbiol 66:97–139
Smith NA, Kelly DP (1988) Oxidation of carbon disulphide as the sole source of energy for the autotrophic growth of Thiobacillus thioparus strain TK-m. J Gen Microbiol 134:3041–3048
Suga H, Hasegawa T, Mitsui H, Kageyama K, Hyakumachi M (2000) Phylogenetic analysis of the phytopathogenic fungus Fusarium solani based on the rDNA-ITS region. Mycol Res 104:1175–1183
Sugawara H, Tanaka N, Miyazaki S (2003) An e-Workbench for the study of microbial diversity: the system design and basic functions. Microbiol Cult Coll 19:59–67
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Torre MADL, Gomez-Alarcon G, Vizcaino C, Garcia MT (1993) Biochemical mechanisms of stone alteration carried out by filamentous fungi living in monuments. Biogeochemistry 19:129–147
Torres AL, Maroulis PJ, Goldberg AB, Bandy AR (1980) Atmospheric OCS measurements on project Gametag. J Geophys Res 85:7357–7360
Vitolins MI, Swaby RJ (1969) Activity of sulphur-oxidizing microorganisms in some Australian soils. Aust J Soil Res 7:171–183
Wainwright M (1970) Sulphur-oxidising micro-organisms on vegetation and in soils exposed to atmospheric pollution. Environ Pollut 17:167–174
Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegrad 46:343–368
Watts SF (2000) The mass budgets of carbonyl sulfide, dimethyl sulfide, carbon disulfide and hydrogen sulfide. Atmos Environ 34:761–779
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA
Wieringa KT (1966) Solid media with elemental sulphur for detection of sulphur-oxidizing microbes. Antonie Leeuwenhoek 32:183–186
Acknowledgements
Assistance of Hideo Arai, Yu Osuga, and Ichita Shimoda in sampling is appreciated. This research was supported by Japanese Government Team for Safeguarding Angkor and a Grant-in-aid for Scientific Research (No.19251001) from The Ministry of Education, Culture, Sports, and Technology of Japan. We thank APSARA Authority and Ministry of Environment, Kingdom of Cambodia, for permission of sampling stone materials.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, X.S., Sato, T., Ooiwa, Y. et al. Oxidation of Elemental Sulfur by Fusarium solani Strain THIF01 Harboring Endobacterium Bradyrhizobium sp.. Microb Ecol 60, 96–104 (2010). https://doi.org/10.1007/s00248-010-9699-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-010-9699-1