Abstract
There is increasing evidence for the presence and activity of methanotrophic bacteria in saline and alkaline aquatic environments located in different ecogeographical regions. Alkalitolerant halophilic and alkaliphilic halotolerant methanotrophs of type I were found to be able to utilize methane and methanol, to oxidize ammonium ions, and to transform various organic compounds in a wide range of water salinities (up to 12% NaCl) and pH values (from 5 to 11). The ecophysiological importance of methanotrophs in microbial communities inhabiting saline and alkaline aquatic environments is due to their involvement in the global cycles of methane and major bioelements (C, N, and S). Specific cyto- and biochemical properties of haloalkaliphilic methanotrophs—the synthesis of osmoprotectants (ectoine, 5-oxoproline, and sucrose), the accumulation of potassium ions, the formation of glycoprotein S-layers on the outer surface of their cell walls, and the modification of the chemical composition of their membranes—allow them to adapt to highly saline and alkaline habitats. Due to their specific properties, haloalkaliphilic methanotrophs may be of use in modern biotechnology.
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REFERENCES
Gal’chenko, V.F., Andreev, L.V., and Trotsenko, Yu.A., Taksonomiya i identifikatsiya obligatnykh metanotrofnykh bakterii(Taxonomy and Identification of Obligately Methanotrophic Bacteria), Pushchino: Nauchn. Tsentr Biol. Issled. Akad. Nauk SSSR, 1986.
Malashenko, Yu.P., Romanovskaya, V.A., and Trotsenko, Yu.A., Metanokislyayushchie mikroorganizmy(Methane-oxidizing Microorganisms), Moscow: Nauka, 1978.
Hanson, R.S. and Hanson, T.E., Methanotrophic Bacteria, Microbiol. Rev., 1996, vol. 60, no. 2, pp. 439-471.
Sieburth, J.M., Jonson, P.W., Eberhardt, M.A., Sieracki, M.E., Lidstrom, M.E., and Laux, D., The First Methane-oxidizing Bacterium from the Upper Mixing Layer of the Deep Ocean: Methylomonas pelagicasp. nov, Curr. Microbiol., 1987, vol. 14, pp. 285-293.
Hutton, W.E. and Zobell, C.E., The Occurrence and Characteristics of Methane-oxidizing Bacteria in Marine Sediments, J. Bacteriol.,1949, vol. 58, no. 4, pp. 463-474.
Lidstrom, M.E., Isolation and Characterization of Marine Methanotrophs, Antonie van Leeuwenhoek, 1988, vol. 54, no. 3, pp. 189-199.
Gal’chenko, V.F., The Bacterial Methane Cycle in Marine Ecosystems, Priroda, 1995, no. 6, pp. 35-48.
Galchenko, V.F., Ecology of Methanotrophic Bacteria in Aquatic Ecosystems, Turpaev, T.M., Ed., New York: Harwood, 1995.
Malashenko, Yu.R., Khaier, Yu., Berger, U., Romanovskaya, V.A., and Muchnik, F.V., Biologiya metanobrazuyushchikh i metanokislyayushchikh mikroorganizmov(The Biology of Methanogenic and Methane-oxidizing Microorganisms), Kiev: Naukova Dumka, 1993.
Malashenko, Yu.R., Khaier, Yu., Romanovskaya, V.A., Berger, U., Budkova, E.N., and Shatokhina, E.S., Formation and Oxidation of Methane in Hypersaline Lakes, Mikrobiol. Zh., 1995, vol. 57, no. 3, pp. 24-29.
Grant, W.D. and Jones, B.E., Alkaline Environments, Encyclopedia of Microbiology,Lederberg, J., Ed., New York: Academic, vol. 1, pp. 126-133.
Issatchenko, B.L., Biogenic Processes in the Chlorine, Sulfate, and Alkaline Lakes of the Kulunda Steppe, Izbrannye trudy(Selected Works), Moscow: Akad. Nauk SSSR, 1951, pp. 143-162.
Zhilina, T.N. and Zavarzin, G.A., Alkaliphilic Anaerobic Community at pH 10, Curr. Microbiol., 1994, vol. 29, no. 2, pp. 109-112.
Zavarzin, G.A., Zhilina, T.N., and Pikuta, E.V., Secondary Anaerobes in the Haloalkaliphilic Communities of Tuva Lakes, Mikrobiologiya, 1996, vol. 65, no. 4, pp. 546-553.
Sorokin, D.Yu., Lysenko, A.M., and Mityushina, L.L., Isolation and Characterization of Alkaliphilic Chemoorganotrophic Bacteria Capable of Oxidizing Reduced Inorganic Sulfur Compounds to Tetrathionate, Mikrobiologiya, 1996, vol. 65, pp. 370-383.
Ventoza, A., Nieto, J.J., and Oren, A., Biology of Moderately Halophilic Aerobic Bacteria, Microbiol. Mol. Biol. Rev., 1998, vol. 62, no. 2, pp. 504-544.
Yumoto, I., Yamasaki, K., Sawabe, T., Nakano, K., Kawasaki, K., Ezura, Y., and Shinano, H., Bacillus hortisp. nov., a New Gram-Negative Alkaliphilic Bacillus, Int. J. Syst. Bacteriol., 1998, vol. 48, pp. 565-571.
Joye, S.B., Connell, T.L., Miller, L.G., Oremland, R.S., and Jellison, R.S., Oxidation of Ammonia and Methane in an Alkaline, Saline Lake, Limnol. Oceanogr., 1999, vol. 44, no. 1, pp. 178-188.
Zavarzin, G.A., Epicontinental Soda Lakes as Possible Relic Biotopes Where Terrestrial Biota Had Evolved, Mikrobiologiya, 1993, vol. 62, no. 5, pp. 789-800.
Zavarzin, G.A., Zhilina, T., and Kevbrin, V.V., Alkaliphilic Microbial Communities and Their Functional Diversity, Mikrobiologiya, 1999, vol. 68, no. 5, pp. 579-599.
Tindall, B.J., Prokaryotic Life in the Alkaline Saline Athalassic Environment, Halophilic Bacteria, Rodrigez-Valera, F., Ed., Boca Raton: CRC, 1988, pp. 31-67.
Jones, B.E., Grant, W.D., Collins, N.C., and Mwatha, W.E., Alkaliphiles: Diversity and Identification, Bacterial Diversity and Systematics, Priest, F.G. et al., Eds., New York: Plenum, 1994, pp. 195-228.
Jones, B.E., Grant, W.D., Duckworth, A.W., and Owenson, G.G., Microbial Diversity of Soda Lakes, Extremophiles, 1998, vol. 2, pp. 191-200.
Gorlenko, V.M., Namsaraev, B.B., Kulyrova, A.V., Zavarzin, D.G., and Zhilina, T.N., Activity of Sulfatereducing Bacteria in the Bottom Sediments of Soda Lakes in the Southeastern Transbaikal Region, Mikrobiologiya, 1999, vol. 68, no. 5, pp. 664-670.
Slobodkin, F.I. and Zavarzin, G.A., Formation of Methane in the Halophilic Cyanobacterial Mats of Syvash, Mikrobiologiya, 1992, vol. 61, no. 2, pp. 294-299.
Conrad, R., Frenzel, P., and Cohen, Y., Methane Emission from Hypersaline Microbial Mats: Lack of Aerobic Methane Oxidation Activity, FEMS Microbiology, 1995, vol. 16, pp. 297-306.
Sokolov, A.P. and Trotsenko, Y.A., Methane Consumption in (Hyper)saline Habitats of the Crimea (Ukraine), FEMS Microbiol. Ecol., 1995, vol. 18, pp. 299-304.
Khmelenina, V.N., Starostina, N.G., Tsvetkova, M.G., Sokolov, A.P., Suzina, N.E., and Trotsenko, Yu.A., Methanotrophic Bacteria in the Saline Lakes of Ukraine and Tuva, Mikrobiologiya, 1996, vol. 65, no. 5, pp. 696-703.
Khmelenina, V.N., Eshinimaev, B.Ts., Kalyuzhnaya, M.G., and Trotsenko, Yu.A., The Potential Activity of Methane and Ammonium Oxidation by the Methanotrophic Communities of Soda Lakes in the Southern Transbaikal Region, Mikrobiologiya, vol. 69, no. 4, pp. 553-558.
Namsaraev, B.B., Zhilina, T.N., Kulyrova, A.V., and Gorlenko, V.M., Bacterial Production of Methane in the Soda Lakes of the Southeastern Transbaikal Region, Mikrobiologiya, 1999, vol. 68, no. 5, pp. 671-676.
Murrell, J.C., McDonald, I.R., and Bourne, D.G., Molecular Methods for the Study of Methanotroph Ecology, FEMS Microbiol. Ecol., 1998, vol. 27, pp. 103-114.
Holmes, A.J., Owens, N.J., and Murrell, J.C., Detection of Novel Marine Methanotrophs Using Phylogenetic and Functional Gene Probes after Methane Enrichment, Microbiology, 1995, vol. 141, no. 8, pp. 1947-1955.
Khmelenina, V.N., Kalyuzhnaya, M.G., Starostina, N.G., Suzina, N.E., and Trotsenko, Y.A., Isolation and Characterization of Halotolerant Alkaliphilic Methanotrophic Bacteria from Tuva Soda Lakes, Curr. Microbiol., 1997, vol. 35, no. 5, pp. 257-261.
Kalyuzhnaya, M.G., Khmelenina, V.N., Starostina, N.G., Baranova, S.V., Suzina, N.E., and Trotsenko, Yu.A., A New Moderately Halophilic Methanotroph of the Genus Methylobacter, Mikrobiologiya, 1998, vol. 67, no. 4, pp. 532-539.
Kalyuzhnaya, M.G., Khmelenina, V.N., Suzina, N.E., Lysenko, A.M., and Trotsenko, Yu.A., New Methanotrophic Bacteria Isolated from the Soda Lakes of Southern Transbaikal, Mikrobiologiya, 1999, vol. 68, no. 5, pp. 689-697.
Kalyuzhnaya, M.G., Khmelenina, V.N., Eshinimaev, B.Ts., Suzina, N.E., Nikitin, D., Solonin, A., Lin, J.L., McDonald, I.R., Murrell, J.C., and Trotsenko, Y.A., Taxonomic Characterization of New Alkaliphilic and Alkalitolerant Methanotrophs from Soda Lakes of the Southeastern Transbaikal Region and Description of Methylomicrobium buryatensesp. nov., Syst. Appl. Microbiol., 2001, vol. 24, pp. 166-176.
Khmelenina, V.N., Kalyuzhnaya, M.G., and Trotsenko, Yu.A., Physiological and Biochemical Characteristics of the Haloalkalitolerant Methanotroph Methylobacter alcaliphilus, Mikrobiologiya, 1997, vol. 66, no. 4, pp. 447-453.
Sorokin, D.Y., Jones, B.E., and Kuenen, J.G., A Novel Obligately Methylotrophic, Methane-oxidizing MethylomicrobiumSpecies from a Highly Alkaline Environment, Extremophiles, 2000, vol. 4, no. 1, pp. 145-155.
Khmelenina, V.N., Kalyuzhnaya, M.G., Sakharovsky, V.G., Trotsenko, Y.A., and Gottschalk, G., Osmoadaptation in Halophilic and Alkaliphilic Methanotrophs, Arch. Microbiol., 1999, vol. 172, no. 5, pp. 321-329.
Severina, L.O., Bacterial S-layers, Mikrobiologiya, 1995, vol. 64, no. 6, pp. 725-733.
Sleytr, U.B. and Beveridge, J., Bacterial S-layers, Trends Microbiol., 1999, vol. 7, no. 6, pp. 253-260.
Tyurin, V.S., Gorskaya, L.A., Kaftanova, A.S., Loginova, T.M., and Mikhailov, A.M., Some Particular Characteristics of the Minute Structure of Methylococcus capsulatusCells under Different Cultivation Conditions, Mikrobiologiya, 1985, vol. 54, no. 6, pp. 770-775.
Russell, N.J., Adaptive Modifications in Membranes of Halotolerant and Halophilic Microorganisms, J. Bioenerg. Biomembr., 1989, vol. 54, no. 1, pp. 93-113.
Thiemann, B. and Imhoff, I.F., The Effect of Salt on the Lipid Composition of Ectothiorhodospira, Arch. Microbiol., 1991, vol. 156, no. 5, pp. 376-384.
Galinski, E.A. and Trüper, H.G., Microbial Behavior in Salt-stressed Ecosystems, FEMS Microbiol. Rev., 1994, vol. 15, pp. 95-108.
Galinski, E.A., Osmoadaptation in Bacteria, Adv. Microb. Physiol., 1995, vol. 37, pp. 273-328.
Costa, M.S., Santos, H., and Galinski, E.A., Solutes in Bacteria and Archaea, Adv. Biochem. Eng. Biotechnol., 1998, vol. 61, pp. 118-153.
Khmelenina, V.N., Sakharovskii, V.G., Reshetnikov, A.S., and Trotsenko, Yu.A., Synthesis of Organic Osmoprotectants in Halophilic and Alkaliphilic Methanotrophs, Mikrobiologiya, vol. 69, no. 4, pp. 465-470.
Shishkina, V.N. and Trotsenko, Y.A., Multiple Metabolic Lesions in Obligate Methanotrophic Bacteria, FEMS Microbiol. Lett., 1982, vol. 13, pp. 237-242.
Peters, P., Galinski, E.A., and Trüper, H.G., The Biosynthesis of Ectoine, FEMS Microbiol. Lett., 1990, vol. 71, no. 1-2, pp. 157-162.
Vorholt, J.A., Chistoserdova, L., Stolyar, S.M., Thauer, R.K., and Lidstrom, M.E., Distribution of Tetrahydromethanopterin-Dependent Enzymes in Methylotrophic Bacteria and Phylogeny of Methenyl Tetrahydromethanopterin Cyclohydrolases, J. Bacteriol., 1999, vol. 181, no. 18, pp. 5750-5757.
Schauder, R., Preuß, A., Jetten, M., and Fuchs, G., Oxidative and Reductive Acetyl CoA/Carbon Monoxide Dehydrogenase Pathway in Desulfobacterium autotrophicum: II. Demonstration of the Enzymes of the Pathway and Comparison of CO Dehydrogenases, Arch. Microbiol., 1989, vol. 151, no. 1, pp. 84-89.
Oren, A., Bioenergetic Aspects of Halophilism, Microbiol. Mol. Biol. Rev., 1999, vol. 63, no. 2, pp. 334-348.
Doronina, N.V., Darmaeva, Ts.D., and Trotsenko, Yu.A., New Aerobic Methylotrophic Isolates from the Soda Lakes of Southern Transbaikal, Mikrobiologiya,2001, vol. 70, no. 3, pp. 398-404.
Kevbrin, V.V., Zhilina, T.N., Rainey, F.A., and Zavarzin, G.A., Tindallia magadiigen. nov., sp. nov., an Alkaliphilic Anaerobic Ammonifier from Soda Lake Deposits, Curr. Microbiol., 1998, vol. 37, pp. 94-100.
Zhilina, T.N., Detkova, E.N., Rainey, F.A., Osipov, G.A., Lysenko, A.M., Kostrikina, N.A., and Zavarzin, G.A., Natronoincola histidinovoransgen. nov., sp. nov., a New Alkaliphilic Acetogenic Anaerobe, Curr. Microbiol., 1998, vol. 37, pp. 177-185.
Ward, B.B., Martino, P.P., Diarz, M.C., and Joe, S.B., Analysis of Ammonia-oxidizing Bacteria from Hypersaline Mono Lake, California, on the Basis of 16S RNA Sequences, Appl. Environ. Microbiol., 2000, vol. 66, no. 7, pp. 2873-2884.
Joye, S.B., Connell, T.L., Miller, L.G., Oremland, R.S., and Jellison, R.S., Oxidation of Ammonia and Methane in an Alkaline, Saline Lake, Limnol. Oceanogr., 1999, vol. 44, no. 1, pp. 178-188.
Fuse, H., Ohta, M., Takimura, O., Murakami, K., Inoue, H., Yamaoka, Y., Oclarit, J.M., and Omori, T., Oxidation of Trichloroethylene and Dimethyl Sulfide by a Marine MethylomicrobiumStrain Containing Soluble Methane Monooxygenase, Biosci. Biotechnol. Biochem., 1998, vol. 62, pp. 1925-1931.
Lippert, K. and Galinski, E.A., Enzyme Stabilization by Ectoine-Type Compatible Solutes: Protection against Heating, Freezing, and Drying, Appl. Microbiol. Biotechnol., 1992, vol. 37, pp. 61-65.
Louis, P., Trüper, H.G., and Galinski, E.A., Survival of Escherichia coliduring Drying and Storage in the Presence of Compatible Solutes, Appl. Microbiol. Biotechnol., 1994, vol. 41, pp. 684-688.
Sleytr, U.B., Basic and Applied S-Layer Research: An Overview, FEMS Microbiol. Rev., 1997, vol. 20, no. 1/2, pp. 5-12.
Kevbrin, V.V., Zhilina, T.N., and Zavarzin, G.A., The Degradation of Cellulose by an Anaerobic Alkaliphilic Microbial Community, Mikrobiologiya, 1999, vol. 68, no. 5, pp. 686-695.
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Trotsenko, Y.A., Khmelenina, V.N. The Biology and Osmoadaptation of Haloalkaliphilic Methanotrophs. Microbiology 71, 123–132 (2002). https://doi.org/10.1023/A:1015183832622
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DOI: https://doi.org/10.1023/A:1015183832622