Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism.
Under sulfur deprivation conditions, the green alga Chlamydomonas reinhardtii produces hydrogen in the light in a sustainable manner thanks to the contribution of two pathways, direct and indirect. In the direct pathway, photosystem II (PSII) supplies electrons to hydrogenase through the photosynthetic electron transport chain, while in the indirect pathway, hydrogen is produced in the absence of PSII through a photosystem I-dependent process. Starch metabolism has been proposed to contribute to both pathways by feeding respiration and maintaining anoxia during the direct pathway and by supplying reductants to the plastoquinone pool during the indirect pathway. At variance with this scheme, we report that a mutant lacking starch (defective for sta6) produces similar hydrogen amounts as the parental strain in conditions of sulfur deprivation. However, when PSII is inhibited by 3-(3,4-dichlorophenyl)-1,1-dimethylurea, conditions where hydrogen is produced by the indirect pathway, hydrogen production is strongly reduced in the starch-deficient mutant. We conclude that starch breakdown contributes to the indirect pathway by feeding electrons to the plastoquinone pool but is dispensable for operation of the direct pathway that prevails in the absence of DCMU. While hydrogenase induction was strongly impaired in the starch-deficient mutant under dark anaerobic conditions, wild-type-like induction was observed in the light. Because this light-driven hydrogenase induction is DCMU insensitive and strongly inhibited by carbonyl cyanide-p-trifluoromethoxyphenylhydrazone or 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, we conclude that this process is regulated by the proton gradient generated by cyclic electron flow around PSI.
Chochois
Vincent
V
Commissariat à l'Energie Atomique, Direction des Sciences du Vivant, Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Bioénergétique et Biotechnologie des Bactéries et Microalgues, Commissariat à l'Energie Atomique Cadarache, F-13108 Saint-Paul-lez-Durance, France.
Dauvillée
David
D
Beyly
Audrey
A
Tolleter
Dimitri
D
Cuiné
Stéphan
S
Timpano
Hélène
H
Ball
Steven
S
Cournac
Laurent
L
Peltier
Gilles
G
D000085:Acetates / Q000378:metabolism; D000693:Anaerobiosis; D000818:Animals; D002696:Chlamydomonas / Q000166:cytology / Q000201:enzymology / Q000378:metabolism*; D003903:Deuterium / Q000378:metabolism; D005816:Genetic Complementation Test; D006859:Hydrogen / Q000378:metabolism*; D006864:Hydrogenase / Q000378:metabolism; D042541:Intracellular Space / Q000378:metabolism; D009154:Mutation / Q000235:genetics; D045332:Photosystem II Protein Complex / Q000378:metabolism*; D013213:Starch / Q000378:metabolism*; D013455:Sulfur / Q000172:deficiency
D000085:Acetates; D045332:Photosystem II Protein Complex; D013455:Sulfur; D006859:Hydrogen; D013213:Starch; D003903:Deuterium; D006864:Hydrogenase
Plant Physiol. 1984 May;75(1):212-8
16663574
J Bacteriol. 2001 Feb;183(3):1069-77
11208806
Trends Biotechnol. 2000 Dec;18(12):506-11
11102662
Eur J Biochem. 2002 Feb;269(3):1022-32
11846805
Appl Microbiol Biotechnol. 2006 Sep;72(3):442-9
16896600
Plant Cell Physiol. 2003 Feb;44(2):146-55
12610217
Plant Physiol. 1986 Sep;82(1):160-6
16664985
Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17548-53
17951433
Biochim Biophys Acta. 2005 Jul 15;1708(3):322-32
15950924
Plant Cell. 1996 Aug;8(8):1353-1366
12239416
Plant Cell. 2004 Aug;16(8):2151-63
15269330
Plant J. 2006 Oct;48(2):274-85
17018036
J Biol Chem. 2009 Feb 13;284(7):4148-57
19056727
Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20546-51
19074271
Plant Physiol. 1978 Jun;61(6):953-6
16660433
Planta. 2008 Jan;227(2):397-407
17885762
Planta. 2007 Oct;226(5):1075-86
17721788
J Bacteriol. 2004 Mar;186(6):1737-46
14996805
Proc Natl Acad Sci U S A. 1990 Feb;87(3):1228-32
2105499
Eur J Biochem. 1994 Jun 15;222(3):769-74
8026490
Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10237-41
7479759
Plant Physiol. 2000 Jan;122(1):127-36
10631256
Plant Physiol. 2001 Nov;127(3):740-8
11706159
Planta. 2002 Feb;214(4):552-61
11925039
Plant Physiol. 2006 Sep;142(1):305-17
16844835
Nature. 2005 Feb 24;433(7028):892-5
15729347
Appl Environ Microbiol. 2005 Oct;71(10):6199-205
16204539
Cell. 2008 Jan 25;132(2):273-85
18243102
Appl Biochem Biotechnol. 1997 Spring;63-65:141-51
18576077
Cell. 2002 Aug 9;110(3):361-71
12176323
Plant Physiol. 1998 May;117(1):129-39
9576782