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The Historical Development of Cultivation Techniques for Methanogens and Other Strict Anaerobes and Their Application in Modern Microbiology

. 2022 Feb 10 ; 10 (2) : . [epub] 20220210

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

Links

PubMed 35208865
PubMed Central PMC8879435
DOI 10.3390/microorganisms10020412
PII: microorganisms10020412
Knihovny.cz E-resources

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.

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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

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