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Characterization of unusual truncated hemoglobins of Chlamydomonas reinhardtii suggests specialized functions

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Abstract

Main conclusion

Annotated hemoglobin genes in Chlamydomonas reinhardtii form functional globins, despite unusual architectures. Spectral characteristics show subtle biochemical differences. Multiple globins might help the alga to cope with its versatile environment.

The unicellular green alga C. reinhardtii is a photosynthetic, often soil-dwelling organism, subjected to a changeable environment in nature. The alga contains 12 genes encoding so-called truncated hemoglobins that feature a two-on-two helical fold instead of the three-on-three helix arrangement of the long-studied vertebrate globins or plant symbiotic and non-symbiotic hemoglobins. In plants, non-symbiotic hemoglobins often play a role in acclimation to stress, and we could show recently that one of the C. reinhardtii globin genes is vital for anoxic growth. Here, three further globin encoding transcripts (Cre16.g661000.t1.1, Cre16.g661300.t2.1 and Cre16.g662750.t1.2) were heterologously expressed along with the recently studied THB1. UV–Vis and X-ray absorption spectroscopy analyses show that the sequences indeed encode functional hemoglobins, despite their uncommon primary sequences, which include long C-termini without any predictable function, or a split heme-binding domain. The proteins show some variations regarding the coordination of the heme iron or the interaction with diatomic ligands, indicating different functionalities. The respective transcripts are not responsive to the nitrogen source, in contrast to results reported for THB1, but they accumulate in darkness. This work advances experimental data on the very large globin family in general, and, more specifically, on hemoglobins in photosynthetic organisms.

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Abbreviations

BVS:

Bond valence sum

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

EXAFS:

Extended X-ray absorption fine structure

Hb:

Hemoglobin

2/2Hb:

Hemoglobin of the 2-on-2-helices fold (“truncated hemoglobin”)

3/3Hb:

Hemoglobin of the 3-on-3-helices (myoglobin-) fold

Mb:

Myoglobin

NOD:

Nitric oxide dioxygenase

qRT-PCR:

Quantitative reverse transcription polymerase chain reaction

RNA-Seq:

RNA sequencing

rTHB/rTHB-s:

Recombinant 2/2Hb/recombinant 2/2Hb lacking the C-terminus

XANES:

X-ray absorption near edge structure

XAS:

X-ray absorption spectroscopy

References

  • Arcovito A, Bonamore A, Hazemann JL, Boffi A, D’Angelo P (2010) Unusual proximal heme pocket geometry in the deoxygenated Thermobifida fusca: a combined spectroscopic investigation. Biophys Chem 147:1–7

    Article  CAS  PubMed  Google Scholar 

  • Arredondo-Peter R, Hargrove MS, Sarath G, Moran JF, Lohrman J, Olson JS, Klucas RV (1997) Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol 115:1259–1266

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Atteia A, van Lis R, Tielens AG, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta 1827:210–223

    Article  CAS  PubMed  Google Scholar 

  • Bianconi A, Congiu-Castellano A, Dell’Ariccia M, Giovannelli A, Burattini E, Durham PJ (1985) Increase of the Fe effective charge in hemoproteins during oxygenation process. Biochem Biophys Res Commun 131:98–102

    Article  CAS  PubMed  Google Scholar 

  • Blaby IK, Blaby-Haas CE, Tourasse N, Hom EF, Lopez D, Aksoy M, Grossman A, Umen J, Dutcher S, Porter M, King S, Witman GB, Stanke M, Harris EH, Goodstein D, Grimwood J, Schmutz J, Vallon O, Merchant SS, Prochnik S (2014) The Chlamydomonas genome project: a decade on. Trends Plant Sci 19:672–680

    Article  CAS  PubMed  Google Scholar 

  • Camargo A, Llamas A, Schnell RA, Higuera JJ, González-Ballester D, Lefebvre PA, Fernández E, Galván A (2007) Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19:3491–3503

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Catalanotti C, Dubini A, Subramanian V, Yang W, Magneschi L, Mus F, Seibert M, Posewitz MC, Grossman AR (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24:692–707

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cooper CE (1999) Nitric oxide and iron proteins. Biochim Biophys Acta 1411:290–309

    Article  CAS  PubMed  Google Scholar 

  • Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO 3rd, Gladwin MT (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9:1498–1505

    Article  CAS  PubMed  Google Scholar 

  • Couture M, Yeh SR, Wittenberg BA, Wittenberg JB, Ouellet Y, Rousseau DL, Guertin M (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 96:11223–11228

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Das TK, Couture M, Lee HC, Peisach J, Rousseau DL, Wittenberg BA, Wittenberg JB, Guertin M (1999) Identification of the ligands to the ferric heme of Chlamydomonas chloroplast hemoglobin: evidence for ligation of tyrosine-63 (B10) to the heme. Biochemistry (Mosc) 38:15360–15368

    Article  CAS  Google Scholar 

  • Das TK, Weber RE, Dewilde S, Wittenberg JB, Wittenberg BA, Yamauchi K, Van Hauwaert ML, Moens L, Rousseau DL (2000) Ligand binding in the ferric and ferrous states of Paramecium hemoglobin. Biochemistry (Mosc) 39:14330–14340

    Article  CAS  Google Scholar 

  • Dau H, Liebisch P, Haumann M (2003) X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers–potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal Bioanal Chem 376:562–583

    Article  CAS  PubMed  Google Scholar 

  • Davidge KS, Dikshit KL (2013) Haemoglobins of Mycobacteria: structural features and biological functions. Adv Microb Physiol 63:147–194

    CAS  PubMed  Google Scholar 

  • de Montaigu A, Sanz-Luque E, Gálvan A, Fernández E (2010) A soluble guanylate cyclase mediates negative signaling by ammonium on expression of nitrate reductase in Chlamydomonas. Plant Cell 22:1532–1548

    Article  PubMed Central  PubMed  Google Scholar 

  • Dent RM, Han M, Niyogi KK (2001) Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii. Trends Plant Sci 6:364–371

    Article  CAS  PubMed  Google Scholar 

  • Duanmu D, Casero D, Dent RM, Gallaher S, Yang W, Rockwell NC, Martin SS, Pellegrini M, Niyogi KK, Merchant SS, Grossman AR, Lagarias JC (2013) Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc Natl Acad Sci USA 110:3621–3626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dubini A, Mus F, Seibert M, Grossman AR, Posewitz MC (2009) Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. J Biol Chem 284:7201–7213

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duff SM, Wittenberg JB, Hill RD (1997) Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands. J Biol Chem 272:16746–16752

    Article  CAS  PubMed  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  CAS  PubMed  Google Scholar 

  • Florencio FJ, Vega JM (1983) Utilization of nitrate, nitrite and ammonium by Chlamydomonas reinhardii: photoproduction of ammonium. Planta 158:288–293

    Article  CAS  PubMed  Google Scholar 

  • Forrester MT, Foster MW (2012) Protection from nitrosative stress: a central role for microbial flavohemoglobin. Free Radic Biol Med 52:1620–1633

    Article  CAS  PubMed  Google Scholar 

  • Freitas TA, Hou S, Alam M (2003) The diversity of globin-coupled sensors. FEBS Lett 552:99–104

    Article  CAS  PubMed  Google Scholar 

  • Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 181:401–404

    Article  PubMed  Google Scholar 

  • Goodman MD, Hargrove MS (2001) Quaternary structure of rice nonsymbiotic hemoglobin. J Biol Chem 276:6834–6839

    Article  CAS  PubMed  Google Scholar 

  • Grossman AR, Karpowicz SJ, Heinnickel M, Dewez D, Hamel B, Dent R, Niyogi KK, Johnson X, Alric J, Wollman FA, Li H, Merchant SS (2010) Phylogenomic analysis of the Chlamydomonas genome unmasks proteins potentially involved in photosynthetic function and regulation. Photosynth Res 106:3–17

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz MC, Seibert M (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol 190:279–288

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168

    Article  CAS  PubMed  Google Scholar 

  • Hanania GI, Yeghiayan A, Cameron BF (1966) Absorption spectra of sperm-whale ferrimyoglobin. Biochem J 98:189–192

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Academic Press, San Diego

    Google Scholar 

  • Harris EH (2001) Chlamydomonas as a Model Organism. Annu Rev Plant Physiol Plant Mol Biol 52:363–406

    Article  CAS  PubMed  Google Scholar 

  • Hebelstrup KH, Shah JK, Igamberdiev AU (2013) The role of nitric oxide and hemoglobin in plant development and morphogenesis. Physiol Plant 148:457–469

    Article  CAS  PubMed  Google Scholar 

  • Hemschemeier A (2013) Photo-bleaching of Chlamydomonas reinhardtii after dark-anoxic incubation. Plant Signal Behav 8:e27263

    Article  PubMed Central  PubMed  Google Scholar 

  • Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    Article  CAS  PubMed  Google Scholar 

  • Hemschemeier A, Casero D, Liu B, Benning C, Pellegrini M, Happe T, Merchant SS (2013a) COPPER RESPONSE REGULATOR1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 25:3186–3211

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hemschemeier A, Düner M, Casero D, Merchant SS, Winkler M, Happe T (2013b) Hypoxic survival requires a 2-on-2 hemoglobin in a process involving nitric oxide. Proc Natl Acad Sci USA 110:10854–10859

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoogewijs D, Ebner B, Germani F, Hoffmann FG, Fabrizius A, Moens L, Burmester T, Dewilde S, Storz JF, Vinogradov SN, Hankeln T (2012) Androglobin: a chimeric globin in metazoans that is preferentially expressed in Mammalian testes. Mol Biol Evol 29:1105–1114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoy JA, Hargrove MS (2008) The structure and function of plant hemoglobins. Plant Physiol Biochem 46:371–379

    Article  CAS  PubMed  Google Scholar 

  • Hughes MN (1999) Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta 1411:263–272

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482

    Article  CAS  PubMed  Google Scholar 

  • Jacobs J, Glanz S, Bunse-Graßmann A, Kruse O, Kück U (2010) RNA trans-splicing: identification of components of a putative chloroplast spliceosome. Eur J Cell Biol 89:932–939

    Article  CAS  PubMed  Google Scholar 

  • Johnson EA, Lecomte JT (2013) The globins of cyanobacteria and algae. Adv Microb Physiol 63:195–272

    CAS  PubMed  Google Scholar 

  • Johnson EA, Lecomte JT (2014) Characterization of the truncated hemoglobin THB1 from protein extracts of Chlamydomonas reinhardtii. F1000Res 3:294

    PubMed Central  PubMed  Google Scholar 

  • Johnson EA, Rice SL, Preimesberger MR, Nye DB, Gilevicius L, Wenke BB, Brown JM, Witman GB, Lecomte JT (2014) Characterization of THB1, a Chlamydomonas reinhardtii truncated hemoglobin: linkage to nitrogen metabolism and identification of lysine as the distal heme ligand. Biochemistry (Mosc) 53:4573–4589

    Article  CAS  Google Scholar 

  • Kakar S, Hoffman FG, Storz JF, Fabian M, Hargrove MS (2010) Structure and reactivity of hexacoordinate hemoglobins. Biophys Chem 152:1–14

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lambertz C, Chernev P, Klingan K, Leidel N, Sigfridsson KGV, Happe T, Haumann M (2014) Electronic and molecular structures of the active-site H-cluster in [FeFe]-hydrogenase determined by site-selective X-ray spectroscopy and quantum chemical calculations. Chem Sci 5:1187–1203

    Article  CAS  Google Scholar 

  • Le Borgne F, Pruvost J (2013) Investigation and modeling of biomass decay rate in the dark and its potential influence on net productivity of solar photobioreactors for microalga Chlamydomonas reinhardtii and cyanobacterium Arthrospira platensis. Bioresour Technol 138:271–276

    Article  PubMed  Google Scholar 

  • Leidel N, Chernev P, Havelius KG, Schwartz L, Ott S, Haumann M (2012) Electronic structure of an [FeFe] hydrogenase model complex in solution revealed by X-ray absorption spectroscopy using narrow-band emission detection. J Am Chem Soc 134:14142–14157

    Article  CAS  PubMed  Google Scholar 

  • Lima FA, Penfold TJ, van der Veen RM, Reinhard M, Abela R, Tavernelli I, Rothlisberger U, Benfatto M, Milne CJ, Chergui M (2014) Probing the electronic and geometric structure of ferric and ferrous myoglobins in physiological solutions by Fe K-edge absorption spectroscopy. Phys Chem Chem Phys 16:1617–1631

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Thorp HH (1993) Bond valence sum analysis of metal-ligand bond lengths in metalloenzymes and model complexes. 2. Refined distances and other enzymes. Inorg Chem 32:4102–4105

    Article  CAS  Google Scholar 

  • Loppes R, Radoux M, Ohresser MC, Matagne RF (1999) Transcriptional regulation of the Nia1 gene encoding nitrate reductase in Chlamydomonas reinhardtii: effects of various environmental factors on the expression of a reporter gene under the control of the Nia1 promoter. Plant Mol Biol 41:701–711

    Article  CAS  PubMed  Google Scholar 

  • Magneschi L, Catalanotti C, Subramanian V, Dubini A, Yang W, Mus F, Posewitz MC, Seibert M, Perata P, Grossman AR (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol 158:1293–1305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225–229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martínková M, Kitanishi K, Shimizu T (2013) Heme-based globin-coupled oxygen sensors: linking oxygen binding to functional regulation of diguanylate cyclase, histidine kinase, and methyl-accepting chemotaxis. J Biol Chem 288:27702–27711

    Article  PubMed Central  PubMed  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nardini M, Pesce A, Milani M, Bolognesi M (2007) Protein fold and structure in the truncated (2/2) globin family. Gene 398:2–11

    Article  CAS  PubMed  Google Scholar 

  • Ouellet H, Ouellet Y, Richard C, Labarre M, Wittenberg B, Wittenberg J, Guertin M (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci USA 99:5902–5907

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Perazzolli M, Romero-Puertas MC, Delledonne M (2006) Modulation of nitric oxide bioactivity by plant haemoglobins. J Exp Bot 57:479–488

    Article  CAS  PubMed  Google Scholar 

  • Perutz MF (1979) Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu Rev Biochem 48:327–386

    Article  CAS  PubMed  Google Scholar 

  • Pesce A, Bolognesi M, Nardini M (2013) The diversity of 2/2 (truncated) globins. Adv Microb Physiol 63:49–78

    CAS  PubMed  Google Scholar 

  • Petersen MG, Dewilde S, Fago A (2008) Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions. J Inorg Biochem 102:1777–1782

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Philipps G, Krawietz D, Hemschemeier A, Happe T (2011) A pyruvate formate lyase-deficient Chlamydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen production in green algae. Plant J 66:330–340

    Article  CAS  PubMed  Google Scholar 

  • Pin S, Alpert B, Michalowicz A (1982) An investigation by iron K-edge spectroscopy of the oxidation state of iron in hemoglobin and its subunits. FEBS Lett 147:106–110

    Article  CAS  PubMed  Google Scholar 

  • Rassaf T, Flogel U, Drexhage C, Hendgen-Cotta U, Kelm M, Schrader J (2007) Nitrite reductase function of deoxymyoglobin: oxygen sensor and regulator of cardiac energetics and function. Circ Res 100:1749–1754

    Article  CAS  PubMed  Google Scholar 

  • Reeder BJ (2010) The redox activity of hemoglobins: from physiologic functions to pathologic mechanisms. Antioxid Redox Signal 13:1087–1123

    Article  CAS  PubMed  Google Scholar 

  • Rochaix JD (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29:209–230

    Article  CAS  PubMed  Google Scholar 

  • Sainz M, Pérez-Rontomé C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M (2013) Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. Plant J 76:875–887

    Article  CAS  PubMed  Google Scholar 

  • Sanz-Luque E, Ocaña-Calahorro F, Llamas A, Galván A, Fernández E (2013) Nitric oxide controls nitrate and ammonium assimilation in Chlamydomonas reinhardtii. J Exp Bot 64:3373–3383

    Article  CAS  PubMed  Google Scholar 

  • Sanz-Luque E, Ocaña-Calahorro F, de Montaigu A, Chamizo-Ampudia A, Llamas A, Galván A, Fernández E (2015) THB1, a truncated hemoglobin, modulates nitric oxide levels and nitrate reductase activity. Plant J 81:467–479

    Article  CAS  PubMed  Google Scholar 

  • Schreiter ER, Rodriguez MM, Weichsel A, Montfort WR, Bonaventura J (2007) S-nitrosylation-induced conformational change in blackfin tuna myoglobin. J Biol Chem 282:19773–19780

    Article  CAS  PubMed  Google Scholar 

  • Sharma VS, Geibel JF, Ranney HM (1978) “Tension” on heme by the proximal base and ligand reactivity: conclusions drawn from model compounds for the reaction of hemoglobin. Proc Natl Acad Sci USA 75:3747–3750

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sinclair R, Hallam S, Chen M, Chance B, Powers L (1996) Active site structure in cytochrome c peroxidase and myoglobin mutants: effects of altered hydrogen bonding to the proximal histidine. Biochemistry (Mosc) 35:15120–15128

    Article  CAS  Google Scholar 

  • Smagghe BJ, Trent JT 3rd, Hargrove MS (2008) NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLoS One 3:e2039

    Article  PubMed Central  PubMed  Google Scholar 

  • Stone JR, Marletta MA (1994) Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry (Mosc) 33:5636–5640

    Article  CAS  Google Scholar 

  • Sturms R, DiSpirito AA, Hargrove MS (2011) Plant and cyanobacterial hemoglobins reduce nitrite to nitric oxide under anoxic conditions. Biochemistry (Mosc) 50:3873–3878

    Article  CAS  Google Scholar 

  • Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9:1514–1532

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57:151–168

    Article  CAS  PubMed  Google Scholar 

  • Tinajero-Trejo M, Shepherd M (2013) The globins of Campylobacter jejuni. Adv Microb Physiol 63:97–145

    CAS  PubMed  Google Scholar 

  • Tiso M, Tejero J, Basu S, Azarov I, Wang X, Simplaceanu V, Frizzell S, Jayaraman T, Geary L, Shapiro C, Ho C, Shiva S, Kim-Shapiro DB, Gladwin MT (2011) Human neuroglobin functions as a redox-regulated nitrite reductase. J Biol Chem 286:18277–18289

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vinogradov SN, Moens L (2008) Diversity of globin function: enzymatic, transport, storage, and sensing. J Biol Chem 283:8773–8777

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov SN, Fernández I, Hoogewijs D, Arredondo-Peter R (2011) Phylogenetic relationships of 3/3 and 2/2 hemoglobins in Archaeplastida genomes to bacterial and other eukaryote hemoglobins. Mol Plant 4:42–58

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov SN, Bailly X, Smith DR, Tinajero-Trejo M, Poole RK, Hoogewijs D (2013a) Microbial eukaryote globins. Adv Microb Physiol 63:391–446

    CAS  PubMed  Google Scholar 

  • Vinogradov SN, Tinajero-Trejo M, Poole RK, Hoogewijs D (2013b) Bacterial and archaeal globins—a revised perspective. Biochim Biophys Acta 1834:1789–1800

    Article  CAS  PubMed  Google Scholar 

  • Vojtěchovský J, Chu K, Berendzen J, Sweet RM, Schlichting I (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys J 77:2153–2174

    Article  PubMed Central  PubMed  Google Scholar 

  • Vuletich DA, Lecomte JT (2006) A phylogenetic and structural analysis of truncated hemoglobins. J Mol Evol 62:196–210

    Article  CAS  PubMed  Google Scholar 

  • Wakasugi K, Nakano T, Morishima I (2003) Oxidized human neuroglobin acts as a heterotrimeric Gα protein guanine nucleotide dissociation inhibitor. J Biol Chem 278:36505–36512

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Gau B, Slade WO, Juergens M, Li P, Hicks LM (2014) The global phosphoproteome of Chlamydomonas reinhardtii reveals complex organellar phosphorylation in the flagella and thylakoid membrane. Mol Cell Proteomics 13:2337–2353

    Article  CAS  PubMed  Google Scholar 

  • Wei L, Derrien B, Gautier A, Houille-Vernes L, Boulouis A, Saint-Marcoux D, Malnoë A, Rappaport F, de Vitry C, Vallon O, Choquet Y, Wollman FA (2014) Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26:353–372

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Westre TE, Kennepohl P, DeWitt JG, Hedman B, Hodgson KO, Solomon EI (1997) A Multiplet Analysis of Fe K-Edge 1 s → 3d Pre-Edge Features of Iron Complexes. J Am Chem Soc 119:6297–6314

    Article  CAS  Google Scholar 

  • Wilson SA, Green E, Mathews II, Benfatto M, Hodgson KO, Hedman B, Sarangi R (2013) X-ray absorption spectroscopic investigation of the electronic structure differences in solution and crystalline oxyhemoglobin. Proc Natl Acad Sci USA 110:16333–16338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang W, Catalanotti C, D’Adamo S, Wittkopp TM, Ingram-Smith CJ, Mackinder L, Miller TE, Heuberger AL, Peers G, Smith KS, Jonikas MC, Grossman AR, Posewitz MC (2014) Alternative acetate production pathways in Chlamydomonas reinhardtii during dark anoxia and the dominant role of chloroplasts in fermentative acetate production. Plant Cell 26:4499–4518

    Article  CAS  PubMed  Google Scholar 

  • Zabinsky SI, Rehr JJ, Ankudinov A, Albers RC, Eller MJ (1995) Multiple-scattering calculations of X-ray-absorption spectra. Phys Rev B: Condens Matter 52:2995–3009

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the Deutsche Forschungsgemeinschaft (DFG) for funding (He5790/1-1 and -2, and He5790/3-1 to A.H. and Ha3265/6-1 to M.H.). The work in Bochum was further supported by the Deutsches Zentrum für Luft- und Raumfahrt (DLR) (ModuLES). M.H. gratefully acknowledges the German Bundesministerium für Bildung und Forschung for funding within the Röntgen-Angström Cluster (Grant 05K14KE1), support within Unicat (Cluster of Excellence Berlin), and thanks the DFG for a Heisenberg Fellowship. We thank H. Dau (FU-Berlin) for access to XAS equipment at BESSY, F. Schäfers and M. Mertin for technical support at beamline KMC-1 of BESSY (HZB), and Simon Ernst, Siv Herbrig and Melis Düner for technical assistance at Bochum.

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  1. Work Group Photobiotechnology, Department of Plant Biochemistry, Faculty of Biology and Biotechnology, Ruhr-University of Bochum, Universitätsstr. 150, ND2/134, 44801, Bochum, Germany

    Dennis Huwald & Anja Hemschemeier

  2. Institut für Experimentalphysik, Freie Universität Berlin, Arnimallee 14, 14195, Berlin, Germany

    Peer Schrapers, Ramona Kositzki & Michael Haumann

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  1. Dennis Huwald
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  2. Peer Schrapers
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  3. Ramona Kositzki
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  4. Michael Haumann
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  5. Anja Hemschemeier
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Correspondence to Anja Hemschemeier.

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Huwald, D., Schrapers, P., Kositzki, R. et al. Characterization of unusual truncated hemoglobins of Chlamydomonas reinhardtii suggests specialized functions. Planta 242, 167–185 (2015). https://doi.org/10.1007/s00425-015-2294-4

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  • DOI: https://doi.org/10.1007/s00425-015-2294-4

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