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Hydrogen Metabolism in Aerobic Hydrogen-Oxidizing Bacteria

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Hydrogen metabolism in aerobic hydrogen-oxidizing bacteria. Bernhard SCHINK and Hans-Giinter SCH~LEGEL. Institut [i~r Mikrobiologie der Gesellscha[t [iir Strahlen- und Umwelt[orschung mbH Miinchen, und der Universitiit G6ttingen, 3400 G6ttingen, Grisebachstr. 8, Federal Republic o[ Gerlnany. R~sum~. Summary. On rencontre deux types d'hydroq6nases A survey on orqanisms able to use mole- dans les bact6ries a6robies capables d'oxyder cular hydroqen as electron donor in the enerqy- l'hydroq~ne mol6culaire : les unes sont solubles yieldinq process is presented. In the cyroup of et r6duisent le NAD (H~: NAD oxydor~duc- the aerobic hydroqen-oxidizing bacteria so far rases), les autres sont membranaires et ne two types of hydroqenases have been en- r6duisent pas les pyridine-nucl6otides. Les bac- countered, a NAD-reducinq, soluble enzyme t6ries qui oxydeni l'hydroq~ne peuvent ~tre (H2 : NAD oxidoreductase) and a membrane- divis6es en trois qroupes suivant qu'elles con- bound enzyme unable to reduce pyridine tiennent (i) les deux types d'enzymes (A/ca- nucleotides. With respect to the distribution of liqenes eutrophus), (ii) settlement une enzyme both types of hydroqenases three qroups of soluble (Nocardia opaca lb), (iii) seulement hydroqen-oxidizinq bacteria can be diffen- une enzyme membranaire (la majorit~ des tiated containinq (i) both types (Alcaliqenes qenres et des esp~ces). Nous r6sumons les eutrophus), (ii) a soluble enzyme only (Nocar- 6tudes faites sur l'enzyme & NAD de A. eutro- dia opaca lb), and (iii) a membrane-bound phus. Les r6sultats concernant la solubilisation hydroqenase only (majority of genera and et la purification de l'hydroq6nase membra- species). The results of studies on the NAD- naire de A. eutrophus sont pr6sent6s en d6tail. specific hydroqenase of A. eutrophus are L'enzyme a 6t6 solubilis6e & partir de mem- summarized. Results on the solubilization branes purifi6es & raide de Triton X-100 et de and purification of the membrane-bound hydro- d6soxycholate ou de phespholipase D. L'extrait qenase of A. eutrophus are presented in detail. membranaire brut a 6t6 fractionn6 par pr6ci- The enzyme was solubilized from purified pitation au sulfate d'ammonium et chromato- membranes by Triton X-100 and sodium desoxy- qraphie sur carboxym6thylcellulose & pH 5,5. cholate or phospholipase D. The crude mem- L'enzyme est stable en tampon phosphate ; brane extract was fractionated by ammonium sa stabilit6 en milieu oxydant est comparable sulfate precipitation and chromatography on & celle de l'enzyme soluble. Des donn6es bio- carboxymethylcellulose at pH 5.5. The enzyme chimiques et immunoloqiques indiquent cepen- was stable in potassium phosphate buffer ; dant que les deux enzymes poss~dent des struc- it resembles the soluble enzyme with respect tures diff6rentes. to stability under oxidizinq conditions. Further biochemical and immunoloqical data indicate, however, that both enzymes are different with respect to their native structure. Several metabolic types of organisms are able use hydrogen for aerobic respiration and the to use molecular hydrogen (dihydrogen or H 2) as reduction of carbon dioxide. The second group, an electron donor in the energy-yielding process. which is able to utilize hydrogen under anaerobic Two groups have to be considered. The first group conditions only, comprises various metabolic comprises bacteria utilizing hydrogen under aero- types, chemotrophic as well as phototrophic bac- bic conditions. These are the cheumlithoauto- teria. The chemotrophic hydrogen-utilizing bac- trophic, aerobic hydrogen-oxidizing bacteria teria are the methanogenic bacteria (e.g., Metha- (e.g. Alcaligenes eutrophus); they are able to nosarcina barkeri), the acetogenic bacteria (e.g., 21 298 Ci'ostridium aceticum and Acetobaclerium woodii), energy and on the level, at which the electrons the sulfate-reducing bacteria (e.g., Desul[ovibrio enter the respiratory chain; HJCO 2 ratios of 4 vulgaris) , the nitrate-reducing, denitrifying bac- to 19 have been measured. The average ratio mea- teria (e.g. Paracoccus denitri[icans) and the fuma- sured with Alcaligenes eatrophas is represented rate-reducing bacteria (e.g., Escherichia colt). in equation 3. Among the phototrophic bacteria there are at least 2 H 2 + 02 )'2 H20 (1) some species able to grow with hydrogen as an 2 ~ + C09 ~-<CH20 > + H20 (2) electron donor in each of the lnajor families, fi H 2 + 2 02 + CO 2 ><CH20> +~5 H20 (3) Chromatiaceae (e.g., Chromatium vinosam, Thio- Carbon dioxide tixation occurs via the ribu- capsa roseopersicina), Rhodospirillaceae (e.g., losebisphosphate cycle. So far, anmng the aerobic Rhodospirillum rubrum, Rhodopseudomonas cap- autotrophs no member has been found which assi- sulata) and Chlorobiaceae (e.g., Chlorobium limi- milates CO 2 via another pathway. Thus, the spec- cola var. thiosalphatophilum). Some cyanobacteria tacular ability of the aerobic hydrogen-oxidizing and a few green algae can be adapted to use bacteria to grow with H 2 + CO 2 as the sole energy hydrogen for anoxygenic photosynthesis. The and carbon substrates is due to the combination carbon source used together with hydrogen is of CO~ fixation and hydrogen oxidation, with carbon dioxide, at least in the majority of the ribulosebisphosphate carboxylase, phosphoribulo- bacteria using H 2 as source of reducing power Ikinase and hydrogenase(s) as the main key en- and energy; only the sulfate- and the fumarate- zymes. Otherwise, the hydrogen bacteria are not reducing bacteria lack the ability to fix CO 2 auto- different from normal heterotrophic bacteria; trophically. they are able to grow on organic substrates as well. Taxonomically the aerobic hydrogen-oxidizing There are many bacteria that are able to activate bacteria are a heterogeneous group containing hydrogen in addition to those mentioned. They Gram-negative genera, such as Alcaligenes, Pseu- share the presence of hydrogenases, as the en- domonas, Paracoccus, Aquaspiril?um, Flavobacte- zymes activating or/and releasing hydrogen gas rium, Corynebacterium as well as Gram-positive are collectively called. For example, all nitrogen- genera such as Nocardia, Mycobacterium and fixing bacteria, the rhizobia included, possess Bacillus ([2] ; Aragno and Schlegel, in prepara- hydrogenases ; it is assumed that in these bacteria tion). hydrogenase recycles the hydrogen evolved by nitrogenase thus preventing waste of energy and Hydrogenases, their distribulion and regulation. protecting the nitrogenase from inactivation by oxygen [1]. The obvious questions related to Hydrogenase is the collective name of a multi- hydrogen utilization for energy generation by tude of enzymes either activating or releasing non-autotrophic bacteria have not been definitely hydrogen. In most cases neither the physiological resolved. electron acceptor nor the properties of the en- zymes are known [3]. Some hydrogenases reduce This report will deal with the first group only, N~AD, others ferredoxin, menaquinone or cyto- the aerobic chemoautotrophic bacteria, hereafter chrome c ; the ability to reduce some redox dyes plainly called the hydrogen-oxidizing bacteria. is common to all hydrogenases. These bacteria comprise a physiological group; So far two types of hydrogenase have been en- they are facultatively autotrophic bacteria and countered in the aerobic hydrogen-oxidizing bac- share the ability to grow with hydrogen as elec- teria. The one is a NAD-reducing, soluble enzyme tron donor and with carbon dioxide as the sole (H~ : N,~D oxidoreductase) and the other is a mem- carbon source. brane-bound enzyme unable to reduce pyridine The stoichiometry of the consumption of the nucleotides. With respect to the distribution of gaseous substrates by these bacteria is dependent both types of hydrogenases three groups of hydro- on the growth conditions and growth rate and gen-oxidizing bacteria can be differentiated varies from strain to strain. Hydrogen is used (table I) : in the oxygen-hydrogen reaction serving the gene- (i) Alcaligenes eutrophus [4], A. ruhlandii, [5] ration of ener~ (equation 1) and in the fixation and Pseudomonas saccharophila [6] contain both of CO 2 to the level of cellular material (equation 2). types, the soluble and the membrane-hound hydro- The ratio of hydrogen uptake over the uptake of genase ; (it) Nocardia opaca lb (7) and some fur- carbon dioxide (H2/CO 2) by a suspension of ther species of the genus Nocardia contain a growing cells is dependent on the efficiency of soluble, NAD-reducing enzyme only; (iii) the coupling, on the expenditure for maintenance majority of the hydrogen-oxidizing bacteria, such 299 as Alcaligenes latus, Aquaspirillum aulolrophicum, (Entner-Doudoroff) enzymes is repressed [11]. Paracoccus den itri[icans, several pseudomonads In contrast, in Paracoccus denitri[icans glucose and the coryneform nitrogen-fixing strains, con- is the dominant substrate, and hydrogenase for- tain only a membrane-bound hydrogenase [8]. mation is repressed E12~. The latter type of regu- TABLE I. Hydrogen-oxidizing bacteria and the localization o[ hydrogenases. Hydrogenase Species membrane- nitrogen Gram soluble bound fixation stain Alcaligenes eutrophus dt- Alcaligenes paradoxus 71_ __ w Alcaligenes ruhlandii .~- Alealigenes latus .ql- -- -- Pseudomonas [acilis -AI- -- -- Pseudomonas saccharophila d[_ -q- -- -- Pseudomonas carboxydooorans q.- --- -- Pseudomonas pseudoflava -q.- -- -- Pseudomonas palleronii -q- -- -- Pseudomonas hydrogenooora "JI- -- -- Pseudomonas hgdrogenothermophila Flavobacterium autothermophilum
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  • Electron Donor and Acceptor Utilization by Halorespiring Bacteria'

    Electron Donor and Acceptor Utilization by Halorespiring Bacteria'

    Electron donor andaccepto r utilizationb y halorespiring bacteria Maurice L.G.C. Luijten CENTRALS LANDBOUWCATALOGUS 0000 0950 9080 Promotoren Prof.dr .W.M . de Vos Hoogleraar ind eMicrobiologi c Wageningen Universiteit Prof.dr .ir .A.J.M .Stam s Persoonlijk hoogleraar bij hetlaboratoriu mvoo r Microbiologic Laboratorium voor Microbiologic, Wageningen Universiteit Copromotoren Dr.G .Schra a Universitair docent Laboratorium voor Microbiologic, Wageningen Universiteit Dr.A.A.M . Langenhoff Senior researcher/project leader Milieubiotechnologie, TNO-MEP Promotiecommissie Prof. E.J.Bouwe r John's Hopkins University, Baltimore, USA Prof.dr .C .Hollige r EPFL, Lausanne, Switzerland Dr.F .Volkerin g Tauw bv, Deventer, Nederland Prof. dr.ir .W.H . Rulkens Wageningen Universteit Dit onderzoek is uitgevoerd binnen de onderzoekschool SENSE (Netherlands Research School forth e Socio-Economic andNatura l Sciences ofth e Environment). LV''-:- v. •:-:::'.Ifir Electron donor and acceptor utilizationb y halorespiring bacteria Maurice L.G.C.Luijte n Proefschrift Terverkrijgin g van de graadva n doctor opgeza gva n derecto r magnificus van Wageningen Universiteit, prof. dr. ir. L. Speelman, inhe t openbaar te verdedigen opvrijda g 11 juni 2004 desnamiddag s te half twee in deAula . \ '\ i ocXi ^ Electron donor and acceptor utilization byhalorespirin g bacteria Maurice L.G.C. Luijten Ph.D.thesi sWageninge n University, Wageningen, The Netherlands 2004 ISBN 90-5804-067-1 Front cover: Modified EMpictur e ofSulfurospirillum halorespirans PCE-M2 — ry ' Stellingen 1.El k nadeel heb zijn voordeel. Dit proefschrift. 2. De ene volledige reductie van PCE is de andere nog niet. Dit proefschrift. 3. Sectorale communicatie reikt niet ver genoeg. HRH the Prince of Orange, Wat.