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Cell Proliferation at 122°C and Isotopically Heavy CH4 Production by a Hyperthermophilic Methanogen Under High-Pressure Cultivation

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Cell Proliferation at 122°C and Isotopically Heavy CH4 Production by a Hyperthermophilic Methanogen Under High-Pressure Cultivation Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation Ken Takai*†, Kentaro Nakamura‡, Tomohiro Toki§, Urumu Tsunogai¶, Masayuki Miyazaki*, Junichi Miyazaki*, Hisako Hirayama*, Satoshi Nakagawa*, Takuro Nunoura*, and Koki Horikoshi* *Subground Animalcule Retrieval Program and ‡Institute for Research of Earth Evolution, Japan Agency for Marine–Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan; §Department of Science, Ryukyu University, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan; and ¶Department of Earth and Planetary System Science, Faculty of Science, Hokkaido University, N10 W8, Kita-ku, Sapporo 060-0810, Japan Edited by James M. Tiedje, Michigan State University, East Lansing, MI, and approved May 12, 2008 (received for review January 6, 2008) We have developed a technique for cultivation of chemolithoau- been investigated (13, 14). Other than these studies, investigation totrophs under high hydrostatic pressures that is successfully of methanogens and other chemolithoautotrophs under high applicable to various types of deep-sea chemolithoautotrophs, hydrostatic pressures has been not conducted. including methanogens. It is based on a glass-syringe-sealing liquid Here, we develop a microbiological cultivation and incubation medium and gas mixture used in conjunction with a butyl rubber technique in gas-rich fluid under a high hydrostatic pressure piston and a metallic needle stuck into butyl rubber. By using this corresponding to deep-seafloor and subseafloor habitats. The technique, growth, survival, and methane production of a newly capability of this technique is tested for several indigenous isolated, hyperthermophilic methanogen Methanopyrus kandleri deep-sea chemolithoautotrophs, including a member of the strain 116 are characterized under high temperatures and hydro- genus Methanopyrus, a hyperthermophilic methanogen that had static pressures. Elevated hydrostatic pressures extend the tem- been the most hyperthermophilic microorganism on Earth, perature maximum for possible cell proliferation from 116°C at 0.4 growing in temperatures up to 110°C (15, 16), until Pyrolobus MPa to 122°C at 20 MPa, providing the potential for growth even fumarii (17) and the hyperthermophilic archaeon strain 121 (18) at 122°C under an in situ high pressure. In addition, piezophilic renewed the record of upper temperature limit for life. As growth significantly affected stable carbon isotope fractionation previously reported for M. jannaschii (13) and other hyperther- of methanogenesis from CO2. Under conventional growth condi- tions, the isotope fractionation of methanogenesis by M. kandleri mophilic heterotrophs (19, 20), the piezophilic response to the strain 116 was similar to values (؊34‰ to؊27‰) previously re- elevated hydrostatic pressure can strongly affect the growth ported for other hydrogenotrophic methanogens. However, under physiology, such as temperature ranges of growth and cellular high hydrostatic pressures, the isotope fractionation effect became metabolic and biochemical functions. In this study, the growth, much smaller (<؊12‰), and the kinetic isotope effect at 122°C and survival, and methane production of Methanopyrus kandleri MPa was ؊9.4‰, which is one of the smallest effects ever strain 116, a newly isolated Methanopyrus strain from a deep-sea 40 reported. This observation will shed light on the sources and hydrothermal habitat in the Kairei hydrothermal field in the production mechanisms of deep-sea methane. Central Indian Ridge (CIR Kairei field), are characterized under high hydrostatic pressures equivalent to its potential in situ carbon isotope fractionation ͉ deep-sea hydrothermal vent ͉ habitats. hyperthermophile ͉ methanogenesis ͉ piezophilic Results icrobial methanogenesis in the deep sea is a key process in Development of a Cultivation Technique Under High Hydrostatic Pressures. An easy handling cultivation technique was established Mthe carbon cycle of Earth. It contributes to the CH4 pool (free gas and methane hydrate), a potential energy source and [supporting information (SI) Figs. S1 and S2]. After 3- to 4-day alternative to petroleum (1, 2) as well as a strong greenhouse gas incubations, all of the tested chemolithoautotrophs were suc- with a potential for rapid release (3), in deep-sea and subseafloor cessfully grown in the piezophilic cultivation syringes with final sediments. Methanogens are known to have several methano- cell yields of a level similar to that of those grown under the genic types using different substrates of H2, acetate, methanol, optimum condition without hydrostatic pressure. Thus, our CO, and so on. Hyperthermophilic hydrogenotrophic methano- technique would be applicable to deep-sea and deep-subseafloor gens play a major role in primary production of ecosystems in chemolithoautotrophs with any type of metabolism. deep-sea hydrothermal areas in the present Earth (4, 5) and may represent the most ancient type of microorganisms flourishing in the Archean Earth (6–10). Author contributions: K.T. designed research; K.T., K.N., T.T., U.T., M.M., J.M., H.H., S.N., and T.N. performed research; K.T., K.N., T.T., and U.T. contributed new reagents/analytic Despite the significance of methanogens in the deep-sea and tools; K.T., K.N., T.T., U.T., and M.M. analyzed data; and K.T., K.N., T.T., U.T., and K.H. wrote subseafloor ecosystems, the ecophysiological and biogeochemi- the paper. cal characteristics of their in situ habitats have been little The authors declare no conflict of interest. understood. It has been quite difficult to incorporate high This article is a PNAS Direct Submission. hydrostatic pressures into experiments involving gaseous sub- Freely available online through the PNAS open access option. strates such as H2 and CO2. If this difficulty can be overcome by Data deposition: Methanopyrus kandleri strain 116 was deposited in the Japan Collection any specific apparatus (11, 12), the subsequent handling of of Microorganisms (deposition no. 15049). The 16S rRNA gene sequence of Methanopyrus microbiological experiments under high hydrostatic pressures kandleri strain 116 was deposited in the DDBJ/EMBL/GenBank nucleotide sequence data- remains a great technical barrier. Thus, growth characterization bases (accession no. AB301476). of only thermophilic methanogens Methanocaldococcus jann- †To whom correspondence should be addressed. E-mail: [email protected]. aschii and Methanothermococcus thermolithotrophicus under This article contains supporting information online at www.pnas.org/cgi/content/full/ high pressures has been successfully achieved, and only their 0712334105/DCSupplemental. MICROBIOLOGY piezophilic responses of growth and methane production have © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0712334105 PNAS ͉ August 5, 2008 ͉ vol. 105 ͉ no. 31 ͉ 10949–10954 Downloaded by guest on September 30, 2021 Fig. 1. Cell proliferation curves of M. kandleri strain 116. (A) Under the conventional gas pressure (0.4 MPa). (B) Under the high hydrostatic pressures at 40 or 20 MPa. The data were obtained from different series of experiments. For the cell proliferation curves at 122°C and 40 MPa, patterns from three different series of experiments are shown. Isolation and Taxonomic Characterization of Strain 116. A hyperther- philic cultivation system (Fig. S5). M. kandleri strain 116 was mophilic hydrogenotrophic methanogen, strain 116, was isolated piezophilic, optimally growing at 105°C at hydrostatic pressures from an in situ colonization system deployed in black smoker between 20 and 30 MPa (Fig. S5). The hydrostatic-pressure fluid of the Kairei hydrothermal field (5). Cells of strain116 were range could be equivalent to the in situ hydrostatic pressures of long rods with a width of 0.5–0.7 ␮m and a length of 6–8 ␮m, their potential deep-sea and subseafloor habitats. occurring singly in the exponential growth phase but as filamen- The piezophilic response of M. kandleri strain 116 to the tous forms of up to 20 cells in the stationary growth phase (Fig. growth temperature range was examined. Under a hydrostatic S3). Strain 116 was nonmotile, and no flagellum was observed pressure of 40 MPa, strain 116 grew between 90°C and 122°C, under any growth conditions (Fig. S3). Strain 116 was a hyper- and the optimum temperature for growth was 105°C (Figs. 1 and thermophilic, strictly hydrogenotrophic methanogen that was 2 and Fig. S6). At 122°C and 40 MPa, strain 116 showed a not able to use any methanogenic substrates other than H2 and potential for several rounds of cell division even after 48 h (Fig. CO2. 1). This pattern of cell proliferation at 122°C and 40 MPa was Under a gas pressure of 0.4 MPa, strain 116 grew at 85°C– verified by many different series of experiments (Fig. 1), and the 116°C with an optimum temperature for growth of 100°C (Figs. concomitant methane production according to the cell-number 1 and 2). The optimum pH for growth was 6.3–6.6. Strain 116 increase was identified (Fig. S6 and Tables S1 and S2). The cell required the existence of NaCl for growth in the range 0.5–4.5% proliferation and even the methane production were not de- (wt/vol), and the optimum NaCl concentration was 3.0% (wt/vol). tected in the growth experiment at 123°C (Fig. 1). In addition, Strain 116 used ammonium or nitrate as the sole nitrogen when the growth experiment was conducted at 122°C and 20 source. Selenium, tungsten, and vitamins
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