The Historical Development of Cultivation Techniques for Methanogens and Other Strict Anaerobes and Their Application in Modern Microbiology
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article, Review
Grant support
MUNI/A/1221/2021
Grant Agency of Masaryk University
8J20AT018
Ministry of Education Youth and Sports
PubMed
35208865
PubMed Central
PMC8879435
DOI
10.3390/microorganisms10020412
PII: microorganisms10020412
Knihovny.cz E-resources
- Keywords
- anaerobes, biogas, cultivation methods, methane, methanogens,
- Publication type
- Journal Article MeSH
- Review MeSH
The cultivation and investigation of strictly anaerobic microorganisms belong to the fields of anaerobic microbial physiology, microbiology, and biotechnology. Anaerobic cultivation methods differ from classic microbiological techniques in several aspects. The requirement for special instruments, which are designed to prevent the contact of the specimen with air/molecular oxygen by different means of manipulation, makes this field more challenging for general research compared to working with aerobic microorganisms. Anaerobic microbiological methods are required for many purposes, such as for the isolation and characterization of new species and their physiological examination, as well as for anaerobic biotechnological applications or medical indications. This review presents the historical development of methods for the cultivation of strictly anaerobic microorganisms focusing on methanogenic archaea, anaerobic cultivation methods that are still widely used today, novel methods for anaerobic cultivation, and almost forgotten, but still relevant, techniques.
See more in PubMed
Liu C.-T., Miyaki T., Aono T., Oyaizu H. Evaluation of Methanogenic Strains and Their Ability to Endure Aeration and Water Stress. Curr. Microbiol. 2008;56:214–218. doi: 10.1007/s00284-007-9059-7. PubMed DOI
Hall I.C. Practical Methods in the Purification of Obligate Anaerobes. J. Infect. Dis. 1920;27:576–590. doi: 10.1093/infdis/27.6.576. DOI
Söhngen N.L. Sur Le Rôle Du Méthane Dans La Vie Organique. Recl. Trav. Chim. Pays-Bas Belg. 1910;29:238–274. doi: 10.1002/recl.19100290702. DOI
Veillon A., Zuber A. Recherches Sur Quelques Microbes Strictement Anaérobies et Leur Rôle En Pathologie. Arch. Méd. Exp. Anat. Pathol. 1898;10:517–545.
Wright J.H. A Simple Method Of Cultivating Anaerobic Bacteria. J. Boston Soc. Med. Sci. 1900;5:114–115. PubMed PMC
Ergal İ., Fuchs W., Hasibar B., Thallinger B., Bochmann G., Rittmann S.K.-M.R. The Physiology and Biotechnology of Dark Fermentative Biohydrogen Production. Biotechnol. Adv. 2018;36:2165–2186. doi: 10.1016/j.biotechadv.2018.10.005. PubMed DOI
Kushkevych I., Bosáková V., Vítězová M., Rittmann S.K.-M.R. Anoxygenic Photosynthesis in Photolithotrophic Sulfur Bacteria and Their Role in Detoxication of Hydrogen Sulfide. Antioxidants. 2021;10:829. doi: 10.3390/antiox10060829. PubMed DOI PMC
Mauerhofer L.-M., Zwirtmayr S., Pappenreiter P., Bernacchi S., Seifert A.H., Reischl B., Schmider T., Taubner R.-S., Paulik C., Rittmann S.K.-M.R. Hyperthermophilic Methanogenic Archaea Act as High-Pressure CH4 Cell Factories. Commun. Biol. 2021;4:289. doi: 10.1038/s42003-021-01828-5. PubMed DOI PMC
Rittmann S.K.-M.R., Lee H.S., Lim J.K., Kim T.W., Lee J.-H., Kang S.G. One-Carbon Substrate-Based Biohydrogen Production: Microbes, Mechanism, and Productivity. Biotechnol. Adv. 2015;33:165–177. doi: 10.1016/j.biotechadv.2014.11.004. PubMed DOI
Beigelman P.M., Rantz L.A. Clinical Significance of Bacteroides. Arch. Intern. Med. (Chic). 1949;84:605–631. doi: 10.1001/archinte.1949.00230040084006. PubMed DOI
Veillon A., Zuber A. Sur Quelques Microbes Strictement Anaerobies et Leur Rôle Dans La Pathologie Humaine. Comptes Rendus Hebd. Séances Mém. Soc. Biol. 1897;49:253–255.
Gest H. The Discovery of Microorganisms by Robert Hooke and Antoni van Leeuwenhoek, Fellows of the Royal Society. Notes Rec. R. Soc. Lond. 2004;58:187–201. doi: 10.1098/rsnr.2004.0055. PubMed DOI
Hall I.C. A Review Of The Development And Application Of Physical And Chemical Principles In The Cultivation Of Obligately Anaerobic Bacteria. J. Bacteriol. 1929;17:255–301. doi: 10.1128/jb.17.4.255-301.1929. PubMed DOI PMC
Hungate R.E. Chapter IV A Roll Tube Method for Cultivation of Strict Anaerobes. In: Norris J.R., Ribbons D.W., editors. Methods in Microbiology. Volume 3. Academic Press; Cambridge, MA, USA: 1969. pp. 117–132.
Macy J.M., Snellen J.E., Hungate R.E. Use of Syringe Methods for Anaerobiosis. Am. J. Clin. Nutr. 1972;25:1318–1323. doi: 10.1093/ajcn/25.12.1318. PubMed DOI
Miller T.L., Wolin M.J. A Serum Bottle Modification of the Hungate Technique for Cultivating Obligate Anaerobes. Appl. Microbiol. 1974;27:985–987. doi: 10.1128/am.27.5.985-987.1974. PubMed DOI PMC
Hitchens A.P., Leikind M.C. The Introduction of Agar-Agar into Bacteriology. J. Bacteriol. 1939;37:485–493. doi: 10.1128/jb.37.5.485-493.1939. PubMed DOI PMC
Pasteur L., Faulkner F. Studies on Fermentation: The Diseases of Beer, Their Causes, and the Means of Preventing Them; Macmillan & Company, London, UK, 1879
Sebald M., Hauser D. Pasteur, Oxygen and the Anaerobes Revisited. Anaerobe. 1995;1:11–16. doi: 10.1016/S1075-9964(95)80353-X. PubMed DOI
Finegold S.M. A Century of Anaerobes: A Look Backward and a Call to Arms. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 1993;16((Suppl. 4)):S453–S457. doi: 10.1093/clinids/16.Supplement_4.S453. PubMed DOI
Pasteur L. Scientific Papers: Physiology, Medicine, Surgery, Geology: With Introductions, Notes and Illustrations. Volume 38. Harvard Classics; P.F. Collier & Son; New York, NY, USA: 1910. The Germ Theory And Its Applications To Medicine And Surgery; p. 440.
Hall I.C. Intestinal Flora in New-Born Infants. Am. J. Dis. Child. 1935;49:390–402. doi: 10.1001/archpedi.1935.01970020105010. DOI
Hall I.C. A Constricted Tube with Mechanical Seal for Anaerobic Fermentation Tests. J. Infect. Dis. 1921;29:317–320. doi: 10.1093/infdis/29.4.317. DOI
Griffin A.M. A Modification Of The Buchner Method Of Cultivating Anaerobic Bacteria. Science. 1932;75:416–417. doi: 10.1126/science.75.1946.416. PubMed DOI
Mellon R.R. A Modification of the Wright-Buchner Anaerobic Tube. J. Bacteriol. 1919;4:295–297. doi: 10.1128/jb.4.3.295-297.1919. PubMed DOI PMC
Rockwell G.E. An Improved Method for Anaerobic Cultures. J. Infect. Dis. 1924;35:581–586. doi: 10.1093/infdis/35.6.581. DOI
Heller H.H. Principles Concerning the Isolation of Anaerobes Studies in Pathogenic Anaerobes. Ii. J. Bacteriol. 1921;6:445–470. doi: 10.1128/jb.6.5.445-470.1921. PubMed DOI PMC
Mazé P. Ferment Formenique. Ferment Formenique de l’acetone. Procede de Culture Simple Du Ferment Formenique. C. R. Acad. Sci. 1915;78:398–405.
Anderson B.G. Gaseous Metabolism of Some Anaerobic Bacteria: XIX. Methods. J. Infect. Dis. 1924;35:213–243. doi: 10.1093/infdis/35.3.213. DOI
Lloyd B., Cranston J.A. Studies in Gas Production by Bacteria: Denitrification and Bacterial Growth Phases. Biochem. J. 1930;24:529–548. doi: 10.1042/bj0240529. PubMed DOI PMC
Sacks L.E., Barker H.A. The Influence of Oxygen on Nitrate and Nitrite Reduction. J. Bacteriol. 1949;58:11–22. doi: 10.1128/jb.58.1.11-22.1949. PubMed DOI PMC
Bryant M.P., Burkey L.A. Cultural Methods and Some Characteristics of Some of the More Numerous Groups of Bacteria in the Bovine Rumen. J. Dairy Sci. 1953;36:205–217. doi: 10.3168/jds.S0022-0302(53)91482-9. DOI
Hungate R.E. The Anaerobic Mesophilic Cellulolytic Bacteria. Bacteriol. Rev. 1950;14:1–49. doi: 10.1128/br.14.1.1-49.1950. PubMed DOI PMC
Sowers K.R. Methanogenesis. In: Schaechter M., editor. Encyclopedia of Microbiology. 3rd ed. Academic Press; Oxford, UK: 2009. pp. 265–286.
Hofmann A.W.V.I. On the Action of Trichloride of Phosphorus on the Salts of the Aromatic Monamines. Proc. R. Soc. Lond. 1867;15:54–62. doi: 10.1098/rspl.1866.0018. DOI
Buswell A.M., Hatfield W.D., editors. Anaerobic Fermentations. 32nd ed. Department of Registration and Education, Division of the State Water Supply; Urbana, IL, USA: 1939. Bulletin (Illinois State Water Survey)
Omelianski V.L. Sur La Fermentation Cellulosique. Comptes Rendus Hebd. Séances Mém. Soc. Biol. 1897;125:1131–1133.
Barker H.A. Studies upon the Methane-Producing Bacteria. Arch. Mikrobiol. 1936;7:420–438. doi: 10.1007/BF00407414. DOI
Beijer W.H. Methane Fermentation in the Rumen of Cattle. Nature. 1952;170:576–577. doi: 10.1038/170576a0. PubMed DOI
Barker H.A. Studies upon the Methane Fermentation. IV. The Isolation and Culture of Methanobacterium omelianskii. Antonie Leeuwenhoek. 1939;6:201–220. doi: 10.1007/BF02146187. DOI
Bryant M.P., Wolin E.A., Wolin M.J., Wolfe R.S. Methanobacillus omelianskii, a Symbiotic Association of Two Species of Bacteria. Arch. Mikrobiol. 1967;59:20–31. doi: 10.1007/BF00406313. PubMed DOI
Reddy C.A., Bryant M.P., Wolin M.J. Characteristics of S Organism Isolated from Methanobacillus omelianskii. J. Bacteriol. 1972;109:539–545. doi: 10.1128/jb.109.2.539-545.1972. PubMed DOI PMC
Stadtman T.C., Barker H.A. Studies on the Methane Fermentation. X. A New Formate-Decomposing Bacterium, Methanococcus vannielii. J. Bacteriol. 1951;62:269–280. doi: 10.1128/jb.62.3.269-280.1951. PubMed DOI PMC
Smith P.H., Hungate R.E. Isolation And Characterization Of Methanobacterium ruminantion n. SP1. J. Bacteriol. 1958;75:713–718. doi: 10.1128/jb.75.6.713-718.1958. PubMed DOI PMC
Ferry J.G., Smith P.H., Wolfe R.S. Methanospirillum, a New Genus of Methanogenic Bacteria, and Characterization of Methanospirillum hungatii Sp. Nov. Int. J. Syst. Bacteriol. 1974;24:465–469. doi: 10.1099/00207713-24-4-465. DOI
Zeikus J.G., Henning D.L. Methanobacterium arbophilicum Sp.Nov. An Obligate Anaerobe Isolated from Wetwood of Living Trees. Antonie Leeuwenhoek. 1975;41:543–552. doi: 10.1007/BF02565096. PubMed DOI
Zeikus J.G., Wolfe R.S. Methanobacterium thermoautotrophicus Sp. n., an Anaerobic, Autotrophic, Extreme Thermophile. J. Bacteriol. 1972;109:707–715. doi: 10.1128/jb.109.2.707-713.1972. PubMed DOI PMC
Woese C.R., Fox G.E. Phylogenetic Structure of the Prokaryotic Domain: The Primary Kingdoms. Proc. Natl. Acad. Sci. USA. 1977;74:5088–5090. doi: 10.1073/pnas.74.11.5088. PubMed DOI PMC
Hammes W.P., Winter J., Kandler O. The Sensitivity of the Pseudomurein-Containing Genus Methanobacterium to Inhibitors of Murein Synthesis. Arch. Microbiol. 1979;123:275–279. doi: 10.1007/BF00406661. DOI
Kandler O., König H. Chemical Composition of the Peptidoglycan-Free Cell Walls of Methanogenic Bacteria. Arch. Microbiol. 1978;118:141–152. doi: 10.1007/BF00415722. PubMed DOI
Kates M., Yengoyan L.S., Sastry P.S. A Diether Analog of Phosphatidyl Glycerophosphate in Halobacterium cutirubrum. Biochim. Biophys. Acta BBA—Lipids Lipid Metab. 1965;98:252–268. doi: 10.1016/0005-2760(65)90119-0. PubMed DOI
Kessel M., Klink F. Archaebacterial Elongation Factor Is ADP-Ribosylated by Diphtheria Toxin. Nature. 1980;287:250–251. doi: 10.1038/287250a0. PubMed DOI
Langworthy T.A., Smith P.F., Mayberry W.R. Lipids of Thermoplasma acidophilum. J. Bacteriol. 1972;112:1193–1200. doi: 10.1128/jb.112.3.1193-1200.1972. PubMed DOI PMC
Godsy E.M. Isolation of Methanobacterium bryantii from a Deep Aquifer by Using a Novel Broth-Antibiotic Disk Method. Appl. Environ. Microbiol. 1980;39:1074–1075. doi: 10.1128/aem.39.5.1074-1075.1980. PubMed DOI PMC
König H. Isolation and Characterization of Methanobacterium uliginosum Sp. Nov. from a Marshy Soil. Can. J. Microbiol. 1984;30:1477–1481. doi: 10.1139/m84-235. DOI
Schönheit P., Moll J., Thauer R.K. Growth Parameters (K s, Μmax, Y s) of Methanobacterium thermoautotrophicum. Arch. Microbiol. 1980;127:59–65. doi: 10.1007/BF00414356. PubMed DOI
Stetter K.O. Archaeoglobus Fulgidus Gen. Nov., Sp. Nov.: A New Taxon of Extremely Thermophilic Archaebacteria. Syst. Appl. Microbiol. 1988;10:172–173. doi: 10.1016/S0723-2020(88)80032-8. DOI
Zabel H.P., König H., Winter J. Isolation and Characterization of a New Coccoid Methanogen, Methanogenium tatii Spec. Nov. from a Solfataric Field on Mount Tatio. Arch. Microbiol. 1984;137:308–315. doi: 10.1007/BF00410727. DOI
Balch W.E., Wolfe R.S. New Approach to the Cultivation of Methanogenic Bacteria: 2-Mercaptoethanesulfonic Acid (HS-CoM)-Dependent Growth of Methanobacterium ruminantium in a Pressureized Atmosphere. Appl. Environ. Microbiol. 1976;32:781–791. doi: 10.1128/aem.32.6.781-791.1976. PubMed DOI PMC
Balch W.E., Fox G.E., Magrum L.J., Woese C.R., Wolfe R.S. Methanogens: Reevaluation of a Unique Biological Group. Microbiol. Rev. 1979;43:260–296. doi: 10.1128/mr.43.2.260-296.1979. PubMed DOI PMC
Wolfe R.S. Chapter One—Techniques for Cultivating Methanogens. In: Rosenzweig A.C., Ragsdale S.W., editors. Methods in Enzymology. Volume 494. Academic Press; Cambridge, MA, USA: 2011. pp. 1–22. Methods in Methane Metabolism, Part A. PubMed
Ravichandran M., Munisamy P., Natarajan S.D., Varadharaju C. Rare Detection And Identification of Methanogenic Bacteria from Diverse Ecological Niches in India for Carbon Balance and Management in Our Environment. Int. J. Adv. Res. 2016;4:1174–1186. doi: 10.21474/IJAR01/2508. DOI
Sowers K.R. Growth and Identification. In: Robb F.T., Sowers K.R., DasSarma S., Place A.R., Schreier H.J., Fleischmann E.M., editors. Archaea: A Laboratory Manual—Methanogens. Cold Spring Harbor Laboratory Press; Plainview, NY, USA: 1995. pp. 15–59.
Taubner R.-S., Rittmann S.K.-M.R. Method for Indirect Quantification of CH4 Production via H2O Production Using Hydrogenotrophic Methanogens. Front. Microbiol. 2016;7:532. doi: 10.3389/fmicb.2016.00532. PubMed DOI PMC
Vítězová M., Kohoutová A., Vítěz T., Hanišáková N., Kushkevych I. Methanogenic Microorganisms in Industrial Wastewater Anaerobic Treatment. Processes. 2020;8:1546. doi: 10.3390/pr8121546. DOI
Kotelnikova S., Macario A.J.L., Pedersen K. Methanobacterium subterraneum Sp. Nov., a New Alkaliphilic, Eurythermic and Halotolerant Methanogen Isolated from Deep Granitic Groundwater. Int. J. Syst. Evol. Microbiol. 1998;48:357–367. doi: 10.1099/00207713-48-2-357. PubMed DOI
Pfennig N. Rhodopseudomonas globiformis, Sp. n., a New Species of the Rhodospirillaceae. Arch. Microbiol. 1974;100:197–206. doi: 10.1007/BF00446317. DOI
Widdel F., Kohring G.-W., Mayer F. Studies on Dissimilatory Sulfate-Reducing Bacteria That Decompose Fatty Acids—III. Characterization of the Filamentous Gliding Desulfonema limicola Gen. Nov. Sp. Nov., and Desulfonema magnum Sp. Nov. Arch. Microbiol. 1983;134:286–294. doi: 10.1007/BF00407804. DOI
Widdel F., Bak F. Gram-Negative Mesophilic Sulfate-Reducing Bacteria. In: Balows A., Trüper H.G., Dworkin M., Harder W., Schleifer K.-H., editors. The Prokaryotes. Springer; New York, NY, USA: 1992. pp. 3352–3378.
Cheng L., Dai L., Li X., Zhang H., Lu Y. Isolation and Characterization of Methanothermobacter crinale Sp. Nov., a Novel Hydrogenotrophic Methanogen from the Shengli Oil Field. Appl. Environ. Microbiol. 2011;77:5212–5219. doi: 10.1128/AEM.00210-11. PubMed DOI PMC
Takai K. Methanothermococcus okinawensis Sp. Nov., a Thermophilic, Methane-Producing Archaeon Isolated from a Western Pacific Deep-Sea Hydrothermal Vent System. Int. J. Syst. Evol. Microbiol. 2002;52:1089–1095. doi: 10.1099/ijs.0.02106-0. PubMed DOI
Miller T.L., Wolin M.J. Methanosphaera stadtmaniae Gen. Nov., Sp. Nov.: A Species That Forms Methane by Reducing Methanol with Hydrogen. Arch. Microbiol. 1985;141:116–122. doi: 10.1007/BF00423270. PubMed DOI
Whitman W.B., Ankwanda E., Wolfe R.S. Nutrition and Carbon Metabolism of Methanococcus voltae. J. Bacteriol. 1982;149:852–863. doi: 10.1128/jb.149.3.852-863.1982. PubMed DOI PMC
Morii H., Nishihara M., Koga Y. Isolation, Characterization and Physiology of a New Formate-Assimilable Methanogenic Strain (A2) of Methanobrevibacter arboriphilus. Agric. Biol. Chem. 1983;47:2781–2789. doi: 10.1271/bbb1961.47.2781. DOI
Sprenger W.W., van Belzen M.C., Rosenberg J., Hackstein J.H., Keltjens J.T. Methanomicrococcus blatticola Gen. Nov., Sp. Nov., a Methanol- and Methylamine-Reducing Methanogen from the Hindgut of the Cockroach Periplaneta americana. Int. J. Syst. Evol. Microbiol. 2000;50:1989–1999. doi: 10.1099/00207713-50-6-1989. PubMed DOI
Mauerhofer L.-M., Pappenreiter P., Paulik C., Seifert A.H., Bernacchi S., Rittmann S.K.-M.R. Methods for Quantification of Growth and Productivity in Anaerobic Microbiology and Biotechnology. Folia Microbiol. 2019;64:321–360. doi: 10.1007/s12223-018-0658-4. PubMed DOI PMC
Miller T.L., Lin C. Description of Methanobrevibacter gottschalkii Sp. Nov., Methanobrevibacter thaueri Sp. Nov., Methanobrevibacter woesei Sp. Nov. and Methanobrevibacter wolinii Sp. Nov. Int. J. Syst. Evol. Microbiol. 2002;52:819–822. doi: 10.1099/ijs.0.02022-0. PubMed DOI
Paynter M.J.B., Hungate R.E. Characterization of Methanobacterium mobilis, Sp. n., Isolated from the Bovine Rumen. J. Bacteriol. 1968;95:1943–1951. doi: 10.1128/jb.95.5.1943-1951.1968. PubMed DOI PMC
Rea S., Bowman J.P., Popovski S., Pimm C., Wright A.-D.G. Methanobrevibacter millerae Sp. Nov. and Methanobrevibacter olleyae Sp. Nov., Methanogens from the Ovine and Bovine Rumen That Can Utilize Formate for Growth. Int. J. Syst. Evol. Microbiol. 2007;57:450–456. doi: 10.1099/ijs.0.63984-0. PubMed DOI
Widdel F., Pfennig N. Studies on Dissimilatory Sulfate-Reducing Bacteria That Decompose Fatty Acids: I. Isolation of New Sulfate-Reducing Bacteria Enriched with Acetate from Saline Environments. Description of Desulfobacter postgatei Gen. Nov., Sp. Nov. Arch. Microbiol. 1981;129:395–400. doi: 10.1007/BF00406470. PubMed DOI
Bryant M.P. Commentary on the Hungate Technique for Culture of Anaerobic Bacteria. Am. J. Clin. Nutr. 1972;25:1324–1328. doi: 10.1093/ajcn/25.12.1324. PubMed DOI
Laso-Pérez R., Krukenberg V., Musat F., Wegener G. Establishing Anaerobic Hydrocarbon-Degrading Enrichment Cultures of Microorganisms under Strictly Anoxic Conditions. Nat. Protoc. 2018;13:1310–1330. doi: 10.1038/nprot.2018.030. PubMed DOI
Shlimon A.G. Methanobacterium aarhusense Sp. Nov., a Novel Methanogen Isolated from a Marine Sediment (Aarhus Bay, Denmark) Int. J. Syst. Evol. Microbiol. 2004;54:759–763. doi: 10.1099/ijs.0.02994-0. PubMed DOI
Wolfe R.S., Metcalf W.W. A Vacuum-Vortex Technique for Preparation of Anoxic Solutions or Liquid Culture Media in Small Volumes for Cultivating Methanogens or Other Strict Anaerobes. Anaerobe. 2010;16:216–219. doi: 10.1016/j.anaerobe.2009.11.005. PubMed DOI
Long F., Wang L., Lupa B., Whitman W.B. A Flexible System for Cultivation of Methanococcus and Other Formate-Utilizing Methanogens. Archaea. 2017;2017:e7046026. doi: 10.1155/2017/7046026. PubMed DOI PMC
Stieglmeier M., Wirth R., Kminek G., Moissl-Eichinger C. Cultivation of Anaerobic and Facultatively Anaerobic Bacteria from Spacecraft-Associated Clean Rooms. Appl. Environ. Microbiol. 2009;75:3484–3491. doi: 10.1128/AEM.02565-08. PubMed DOI PMC
Dowell V.R., Hawkins T.M. Laboratory Methods in Anaerobic Bacteriology. CDC Laboratory Manual; Atlanta, GA, USA: 1974.
Nakamura K., Tamaki H., Kang M.S., Mochimaru H., Lee S.-T., Nakamura K., Kamagata Y. A Six-Well Plate Method: Less Laborious and Effective Method for Cultivation of Obligate Anaerobic Microorganisms. Microbes Environ. 2011;26:301–306. doi: 10.1264/jsme2.ME11120. PubMed DOI
Jones W.J., Whitman W.B., Fields R.D., Wolfe R.S. Growth and Plating Efficiency of Methanococci on Agar Media. Appl. Environ. Microbiol. 1983;46:220–226. doi: 10.1128/aem.46.1.220-226.1983. PubMed DOI PMC
Apolinario E.A., Sowers K.R. Plate Colonization of Methanococcus maripaludis and Methanosarcina thermophila in a Modified Canning Jar. FEMS Microbiol. Lett. 1996;145:131–137. doi: 10.1111/j.1574-6968.1996.tb08567.x. DOI
Kiener A., Leisinger T. Oxygen Sensitivity of Methanogenic Bacteria. Syst. Appl. Microbiol. 1983;4:305–312. doi: 10.1016/S0723-2020(83)80017-4. PubMed DOI
Sowers K.R., Boone J.E., Gunsalus R.P. Disaggregation of Methanosarcina Spp. and Growth as Single Cells at Elevated Osmolarity. Appl. Environ. Microbiol. 1993;59:3832–3839. doi: 10.1128/aem.59.11.3832-3839.1993. PubMed DOI PMC
Jones W.J., Leigh J.A., Mayer F., Woese C.R., Wolfe R.S. Methanococcus jannaschii Sp. Nov., an Extremely Thermophilic Methanogen from a Submarine Hydrothermal Vent. Arch. Microbiol. 1983;136:254–261. doi: 10.1007/BF00425213. DOI
Huber H., Thomm M., König H., Thies G., Stetter K.O. Methanococcus thermolithotrophicus, a Novel Thermophilic Lithotrophic Methanogen. Arch. Microbiol. 1982;132:47–50. doi: 10.1007/BF00690816. DOI
Battumur U., Yoon Y., Bae G.S., Kim C.-H. Isolation and Characterization of New Methanosarcina mazei Strains KOR-3, -4, -5, and -6 from an Anaerobic Digester Using Pig Slurry. Asian-Australas. J. Anim. Sci. 2017;30:1198–1205. doi: 10.5713/ajas.16.0830. PubMed DOI PMC
Cuzin N., Labat M., Garcia J.L., Ouattara A.S. Methanobacterium congolense Sp. Nov., from a Methanogenic Fermentation of Cassava Peel. Int. J. Syst. Evol. Microbiol. 2001;51:489–493. doi: 10.1099/00207713-51-2-489. PubMed DOI
Ma K., Liu X., Dong X. Methanobacterium beijingense Sp. Nov., a Novel Methanogen Isolated from Anaerobic Digesters. Int. J. Syst. Evol. Microbiol. 2005;55:325–329. doi: 10.1099/ijs.0.63254-0. PubMed DOI
Dehority B.A. Characterization of Several Bovine Rumen Bacteria Isolated with a Xylan Medium. J. Bacteriol. 1966;91:1724–1729. doi: 10.1128/jb.91.5.1724-1729.1966. PubMed DOI PMC
Chong S.C., Liu Y., Cummins M., Valentine D.L., Boone D.R. Methanogenium marinum Sp. Nov., a H2-Using Methanogen from Skan Bay, Alaska, and Kinetics of H2 Utilization. Antonie Van Leeuwenhoek. 2002;81:263–270. doi: 10.1023/A:1020535222281. PubMed DOI
Krüger M., Beckmann S., Engelen B., Thielemann T., Cramer B., Schippers A., Cypionka H. Microbial Methane Formation from Hard Coal and Timber in an Abandoned Coal Mine. Geomicrobiol. J. 2008;25:315–321. doi: 10.1080/01490450802258402. DOI
Miller N.J., Garrett O.W., Prickett P.S. Anaerobic Technique–a Modified Deep Agar Shake. J. Food Sci. 1939;4:447–451. doi: 10.1111/j.1365-2621.1939.tb17140.x. DOI
Widdel F., Pfennig N. A New Anaerobic, Sporing, Acetate-Oxidizing, Sulfate-Reducing Bacterium, Desulfotomaculum (Emend.) acetoxidans. Arch. Microbiol. 1977;112:119–122. doi: 10.1007/BF00446665. PubMed DOI
Evans J.B., Harrell L.J. Agar Shake Tube Technique for Simultaneous Determination of Aerobic and Anaerobic Susceptibility to Antibioticst. Antimicrob. Agents Chemother. 1977;12:3. doi: 10.1128/AAC.12.4.534. PubMed DOI PMC
Ogg J.E., Lee S.Y., Ogg B.J. A Modified Tube Method for the Cultivation and Enumeration of Anaerobic Bacteria. Can. J. Microbiol. 1979;25:987–990. doi: 10.1139/m79-151. PubMed DOI
Ababouch L., Busta F.F. A Modified Lee Tube Technique for the Cultivation and Enumeration of Anaerobes. Int. J. Food Microbiol. 1986;3:211–216. doi: 10.1016/0168-1605(86)90024-3. DOI
Lee S.Y., Moore S.E., Mabee M.S. Selective-Differential Medium for Isolation and Differentiation of Pectinatus from Other Brewery Microorganisms. Appl. Environ. Microbiol. 1981;41:386–387. doi: 10.1128/aem.41.2.386-387.1981. PubMed DOI PMC
Robertson L.W., Chandrasekaran A., Reuning R.H., Hui J., Rawal B.D. Reduction of Digoxin to 20R-Dihydrodigoxin by Cultures of Eubacterium lentum. Appl. Environ. Microbiol. 1986;51:1300–1303. doi: 10.1128/aem.51.6.1300-1303.1986. PubMed DOI PMC
Hermann M., Noll K.M., Wolfe R.S. Improved Agar Bottle Plate for Isolation of Methanogens or Other Anaerobes in a Defined Gas Atmosphere. Appl. Environ. Microbiol. 1986;51:1124–1126. doi: 10.1128/aem.51.5.1124-1126.1986. PubMed DOI PMC
Olson K.D. Modified Bottle Plate for the Cultivation of Strict Anaerobes. J. Microbiol. Methods. 1992;14:267–269. doi: 10.1016/0167-7012(92)90059-D. DOI
Fröhlich J., König H. Rapid Isolation of Single Microbial Cells from Mixed Natural and Laboratory Populations with the Aid of a Micromanipulator. Syst. Appl. Microbiol. 1999;22:249–257. doi: 10.1016/S0723-2020(99)80072-1. PubMed DOI
Huber R., Huber H., Stetter K.O. Towards the Ecology of Hyperthermophiles: Biotopes, New Isolation Strategies and Novel Metabolic Properties. FEMS Microbiol. Rev. 2000;24:615–623. doi: 10.1111/j.1574-6976.2000.tb00562.x. PubMed DOI
Huser B.A., Wuhrmann K., Zehnder A.J.B. Methanothrix soehngenii Gen. Nov. Sp. Nov., a New Acetotrophic Non-Hydrogen-Oxidizing Methane Bacterium. Arch. Microbiol. 1982;132:1–9. doi: 10.1007/BF00690808. PubMed DOI
Mochimaru H., Tamaki H., Katayama T., Imachi H., Sakata S., Kamagata Y. Methanomicrobium antiquum Sp. Nov., a Hydrogenotrophic Methanogen Isolated from Deep Sedimentary Aquifers in a Natural Gas Field. Int. J. Syst. Evol. Microbiol. 2016;66:4873–4877. doi: 10.1099/ijsem.0.001444. PubMed DOI
Hohnadel M., Maumy M., Chollet R. Development of a Micromanipulation Method for Single Cell Isolation of Prokaryotes and Its Application in Food Safety. PLoS ONE. 2018;13:e0198208. doi: 10.1371/journal.pone.0198208. PubMed DOI PMC
Ishøy T., Kvist T., Westermann P., Ahring B.K. An Improved Method for Single Cell Isolation of Prokaryotes from Meso-, Thermo- and Hyperthermophilic Environments Using Micromanipulation. Appl. Microbiol. Biotechnol. 2006;69:510–514. doi: 10.1007/s00253-005-0014-x. PubMed DOI
Huber R., Burggraf S., Mayer T., Barns S.M., Rossnagel P., Stetter K.O. Isolation of a Hyperthermophilic Archaeum Predicted by in Situ RNA Analysis. Nature. 1995;376:57–58. doi: 10.1038/376057a0. PubMed DOI
Kita A., Suehira K., Miura T., Okamura Y., Aki T., Matsumura Y., Tajima T., Nishio N., Nakashimada Y. Characterization of a Halotolerant Acetoclastic Methanogen Highly Enriched from Marine Sediment and Its Application in Removal of Acetate. J. Biosci. Bioeng. 2016;121:196–202. doi: 10.1016/j.jbiosc.2015.05.018. PubMed DOI
Mori K., Iino T., Suzuki K.-I., Yamaguchi K., Kamagata Y. Aceticlastic and NaCl-Requiring Methanogen “Methanosaeta Pelagica” Sp. Nov., Isolated from Marine Tidal Flat Sediment. Appl. Environ. Microbiol. 2012;78:3416–3423. doi: 10.1128/AEM.07484-11. PubMed DOI PMC
Sowers K.R., Ferry J.G. Isolation and Characterization of a Methylotrophic Marine Methanogen, Methanococcoides methylutens Gen. Nov., Sp. Nov. Appl. Environ. Microbiol. 1983;45:684–690. doi: 10.1128/aem.45.2.684-690.1983. PubMed DOI PMC
Dridi B., Fardeau M.-L., Ollivier B., Raoult D., Drancourt M. The Antimicrobial Resistance Pattern of Cultured Human Methanogens Reflects the Unique Phylogenetic Position of Archaea. J. Antimicrob. Chemother. 2011;66:2038–2044. doi: 10.1093/jac/dkr251. PubMed DOI
Khelaifia S., Drancourt M. Susceptibility of Archaea to Antimicrobial Agents: Applications to Clinical Microbiology. Clin. Microbiol. Infect. 2012;18:841–848. doi: 10.1111/j.1469-0691.2012.03913.x. PubMed DOI
Sakai S., Imachi H., Sekiguchi Y., Tseng I.-C., Ohashi A., Harada H., Kamagata Y. Cultivation of Methanogens under Low-Hydrogen Conditions by Using the Coculture Method. Appl. Environ. Microbiol. 2009;75:4892–4896. doi: 10.1128/AEM.02835-08. PubMed DOI PMC
Imachi H., Sakai S., Sekiguchi Y., Hanada S., Kamagata Y., Ohashi A., Harada H. Methanolinea tarda Gen. Nov., Sp. Nov., a Methane-Producing Archaeon Isolated from a Methanogenic Digester Sludge. Int. J. Syst. Evol. Microbiol. 2008;58:294–301. doi: 10.1099/ijs.0.65394-0. PubMed DOI
Sakai S., Imachi H., Sekiguchi Y., Ohashi A., Harada H., Kamagata Y. Isolation of Key Methanogens for Global Methane Emission from Rice Paddy Fields: A Novel Isolate Affiliated with the Clone Cluster Rice Cluster I. Appl. Environ. Microbiol. 2007;73:4326–4331. doi: 10.1128/AEM.03008-06. PubMed DOI PMC
Sakai S., Imachi H., Hanada S., Ohashi A., Harada H., Kamagata Y. Methanocella paludicola Gen. Nov., Sp. Nov., a Methane-Producing Archaeon, the First Isolate of the Lineage “Rice Cluster I”, and Proposal of the New Archaeal Order Methanocellales Ord. Nov. Int. J. Syst. Evol. Microbiol. 2008;58:929–936. doi: 10.1099/ijs.0.65571-0. PubMed DOI
Mytilinaios I., Salih M., Schofield H.K., Lambert R.J.W. Growth Curve Prediction from Optical Density Data. Int. J. Food Microbiol. 2012;154:169–176. doi: 10.1016/j.ijfoodmicro.2011.12.035. PubMed DOI
Ahn S.-J., Ahn S.-J., Browngardt C.M., Burne R.A. Changes in Biochemical and Phenotypic Properties of Streptococcus Mutans during Growth with Aeration. Appl. Environ. Microbiol. 2009;75:2517–2527. doi: 10.1128/AEM.02367-08. PubMed DOI PMC
Candry P., Van Daele T., Denis K., Amerlinck Y., Andersen S.J., Ganigué R., Arends J.B.A., Nopens I., Rabaey K. A Novel High-Throughput Method for Kinetic Characterisation of Anaerobic Bioproduction Strains, Applied to Clostridium kluyveri. Sci. Rep. 2018;8:9724. doi: 10.1038/s41598-018-27594-9. PubMed DOI PMC
Stringer S.C., Webb M.D., George S.M., Pin C., Peck M.W. Heterogeneity of Times Required for Germination and Outgrowth from Single Spores of Nonproteolytic Clostridium botulinum. Appl. Environ. Microbiol. 2005;71:4998–5003. doi: 10.1128/AEM.71.9.4998-5003.2005. PubMed DOI PMC
Bang C., Schilhabel A., Weidenbach K., Kopp A., Goldmann T., Gutsmann T., Schmitz R.A. Effects of Antimicrobial Peptides on Methanogenic Archaea. Antimicrob. Agents Chemother. 2012;56:4123–4130. doi: 10.1128/AAC.00661-12. PubMed DOI PMC
Weimar M.R., Cheung J., Dey D., McSweeney C., Morrison M., Kobayashi Y., Whitman W.B., Carbone V., Schofield L.R., Ronimus R.S., et al. Development of Multiwell-Plate Methods Using Pure Cultures of Methanogens To Identify New Inhibitors for Suppressing Ruminant Methane Emissions. Appl. Environ. Microbiol. 2017;83 doi: 10.1128/AEM.00396-17. PubMed DOI PMC
Ma L., Kim J., Hatzenpichler R., Karymov M.A., Hubert N., Hanan I.M., Chang E.B., Ismagilov R.F. Gene-Targeted Microfluidic Cultivation Validated by Isolation of a Gut Bacterium Listed in Human Microbiome Project’s Most Wanted Taxa. Proc. Natl. Acad. Sci. USA. 2014;111:9768–9773. doi: 10.1073/pnas.1404753111. PubMed DOI PMC
Villa M.M., Bloom R.J., Silverman J.D., Durand H.K., Jiang S., Wu A., Dallow E.P., Huang S., You L., David L.A. Interindividual Variation in Dietary Carbohydrate Metabolism by Gut Bacteria Revealed with Droplet Microfluidic Culture. mSystems. 2020;5 doi: 10.1128/mSystems.00864-19. PubMed DOI PMC
Watterson W.J., Tanyeri M., Watson A.R., Cham C.M., Shan Y., Chang E.B., Eren A.M., Tay S. Droplet-Based High-Throughput Cultivation for Accurate Screening of Antibiotic Resistant Gut Microbes. eLife. 2020;9:e56998. doi: 10.7554/eLife.56998. PubMed DOI PMC
Steinhaus B., Garcia M.L., Shen A.Q., Angenent L.T. A Portable Anaerobic Microbioreactor Reveals Optimum Growth Conditions for the Methanogen Methanosaeta concilii. Appl. Environ. Microbiol. 2007;73:1653–1658. doi: 10.1128/AEM.01827-06. PubMed DOI PMC
Birgen C., Degnes K.F., Markussen S., Wentzel A., Sletta H. Butanol Production from Lignocellulosic Sugars by Clostridium beijerinckii in Microbioreactors. Biotechnol. Bioeng. 2020;14:1–12. doi: 10.1186/s13068-021-01886-1. PubMed DOI PMC
Widdel F. Grundpraktikum Mikrobiologie, 4. sem. (B. Sc) Universität Bremen; Bremen, Germany: 2007. Theory and Measurement of Bacterial Growth; p. 11.
Azim A.A., Pruckner C., Kolar P., Taubner R.-S., Fino D., Saracco G., Sousa F.L., Rittmann S.K.-M.R. The Physiology of Trace Elements in Biological Methane Production. Bioresour. Technol. 2017;241:775–786. doi: 10.1016/j.biortech.2017.05.211. PubMed DOI
Smith G.C., Floodgate G.D. A Chemical Method for Estimating Methanogenic Biomass. Cont. Shelf Res. 1992;12:1187–1196. doi: 10.1016/0278-4343(92)90078-X. DOI
Widdel F., Wolfe R.S. Expression of Secondary Alcohol Dehydrogenase in Methanogenic Bacteria and Purification of the F420-Specific Enzyme from Methanogenium thermophilum Strain TCI. Arch. Microbiol. 1989;152:322–328. doi: 10.1007/BF00425168. DOI
Shimizu S., Ueno A., Tamamura S., Naganuma T., Kaneko K. Methanoculleus horonobensis Sp. Nov., a Methanogenic Archaeon Isolated from a Deep Diatomaceous Shale Formation. Int. J. Syst. Evol. Microbiol. 2013;63:4320–4323. doi: 10.1099/ijs.0.053520-0. PubMed DOI
Kaesler B., Schönheit P. Methanogenesis and ATP Synthesis in Methanogenic Bacteria at Low Electrochemical Proton Potentials. Eur. J. Biochem. 1988;174:189–197. doi: 10.1111/j.1432-1033.1988.tb14081.x. PubMed DOI
Schönheit P., Beimborn D.B. ATP Synthesis in Methanobacterium thermoautotrophicum Coupled to CH4 Formation from H2 and CO2 in the Apparent Absence of an Electrochemical Proton Potential across the Cytoplasmic Membrane. Eur. J. Biochem. 1985;148:545–550. doi: 10.1111/j.1432-1033.1985.tb08874.x. PubMed DOI
Fukuzaki S., Nishio N., Nagai S. Kinetics of the Methanogenic Fermentation of Acetate. Appl. Environ. Microbiol. 1990;56:3158–3163. doi: 10.1128/aem.56.10.3158-3163.1990. PubMed DOI PMC
Yang S.T., Okos M.R. Kinetic Study and Mathematical Modeling of Methanogenesis of Acetate Using Pure Cultures of Methanogens. Biotechnol. Bioeng. 1987;30:661–667. doi: 10.1002/bit.260300510. PubMed DOI
Pappenreiter P.A., Zwirtmayr S., Mauerhofer L.-M., Rittmann S.K.-M.R., Paulik C. Development of a Simultaneous Bioreactor System for Characterization of Gas Production Kinetics of Methanogenic Archaea at High Pressure. Eng. Life Sci. 2019;19:537–544. doi: 10.1002/elsc.201900035. PubMed DOI PMC
Hanišáková N. Master’s Thesis. Masarykova Universita; Brno, Czechia: 2020. Methanogenic Archaea in Environmental Samples.
Taubner R.-S., Pappenreiter P., Zwicker J., Smrzka D., Pruckner C., Kolar P., Bernacchi S., Seifert A., Krajete A., Bach W., et al. Biological Methane Production under Putative Enceladus-like Conditions. Nat. Commun. 2018;9:748. doi: 10.1038/s41467-018-02876-y. PubMed DOI PMC
Martin M.R., Fornero J.J., Stark R., Mets L., Angenent L.T. A Single-Culture Bioprocess of Methanothermobacter thermautotrophicus to Upgrade Digester Biogas by CO2-to-CH4 Conversion with H2. Archaea. 2013;2013:157529. doi: 10.1155/2013/157529. PubMed DOI PMC
Seifert A.H., Rittmann S., Herwig C. Analysis of Process Related Factors to Increase Volumetric Productivity and Quality of Biomethane with Methanothermobacter marburgensis. Appl. Energy. 2014;132:155–162. doi: 10.1016/j.apenergy.2014.07.002. DOI
Pappenreiter P.A. Ph.D. Thesis. Johannes Kepler University Linz; Linz, Austria: 2020. Development of a Pressurised Biomethanation Reactor System Using CO2-Type Methanogenic Strains.
Bryant M.P., McBride B.C., Wolfe R.S. Hydrogen-Oxidizing Methane Bacteria I. Cultivation and Methanogenesis. J. Bacteriol. 1968;95:1118–1123. doi: 10.1128/jb.95.3.1118-1123.1968. PubMed DOI PMC
Hoffarth M., Broeker T., Schneider J. Effect of N2 on Biological Methanation in a Continuous Stirred-Tank Reactor with Methanothermobacter Marburgensis. Fermentation. 2019;5:56. doi: 10.3390/fermentation5030056. DOI
Mauerhofer L.-M., Reischl B., Schmider T., Schupp B., Nagy K., Pappenreiter P., Zwirtmayr S., Schuster B., Bernacchi S., Seifert A.H., et al. Physiology and Methane Productivity of Methanobacterium thermaggregans. Appl. Microbiol. Biotechnol. 2018;102:7643–7656. doi: 10.1007/s00253-018-9183-2. PubMed DOI PMC
Rittmann S., Seifert A., Herwig C. Quantitative Analysis of Media Dilution Rate Effects on Methanothermobacter marburgensis Grown in Continuous Culture on H2 and CO2. Biomass Bioenergy. 2012;36:293–301. doi: 10.1016/j.biombioe.2011.10.038. DOI
Schill N., van Gulik W.M., Voisard D., von Stockar U. Continuous Cultures Limited by a Gaseous Substrate: Development of a Simple, Unstructured Mathematical Model and Experimental Verification with Methanobacterium thermoautotrophicum. Biotechnol. Bioeng. 1996;51:645–658. doi: 10.1002/(SICI)1097-0290(19960920)51:6<645::AID-BIT4>3.0.CO;2-H. PubMed DOI
Mukhopadhyay B., Johnson E.F., Wolfe R.S. Reactor-Scale Cultivation of the Hyperthermophilic Methanarchaeon Methanococcus jannaschii to High Cell Densities. Appl. Environ. Microbiol. 1999;65:5059–5065. doi: 10.1128/AEM.65.11.5059-5065.1999. PubMed DOI PMC
Shieh J., Whitman W.B. Autotrophic Acetyl Coenzyme A Biosynthesis in Methanococcus maripaludis. J. Bacteriol. 1988;170:3072–3079. doi: 10.1128/jb.170.7.3072-3079.1988. PubMed DOI PMC