A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism

Cell

Volumn 171, Issue 1, 2017, Pages 133-147.e14

  Mackinder, Luke C M ^a,e   Chen, Chris ^a,b   Leib, Ryan D ^b   Patena, Weronika ^a,c   Blum, Sean R ^a,f   Rodman, Matthew ^b   Ramundo, Silvia ^d   Adams, Christopher M ^b   Jonikas, Martin C ^a,b,c  

^a GEOPHYSICAL LABORATORY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF YORK   (United Kingdom)

^f University of California Santa Cruz   (United States)

Author keywords

affinity purification mass spectrometry; carbon fixation; CCM; Chlamydomonas reinhardtii; CO2 concentrating mechanism; high throughput fluorescence protein tagging; photosynthesis; pyrenoid; Rubisco

Indexed keywords

CARBON DIOXIDE; CARBONATE DEHYDRATASE; CARRIER PROTEIN; CELL PROTEIN; RIBULOSEBISPHOSPHATE CARBOXYLASE; ALGAL PROTEIN; CAH6 PROTEIN, CHLAMYDOMONAS REINHARDTII; PHOTOPROTEIN; PLANT PROTEIN;

ARTICLE; CARBON DIOXIDE CONCENTRATING MECHANISM; CARBON DIOXIDE FIXATION; CELL ORGANELLE; CHLAMYDOMONAS REINHARDTII; FLAGELLUM; MASS SPECTROMETRY; NONHUMAN; PHOTOSYSTEM I; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PYRENOID; CARBON CYCLE; CHEMISTRY; CHLOROPLAST; CONFOCAL MICROSCOPY; CYTOLOGY; METABOLISM; PHOTOSYNTHESIS;

ALGAL PROTEINS; CARBON CYCLE; CARBON DIOXIDE; CARBONIC ANHYDRASES; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; PHOTOSYNTHESIS; PLANT PROTEINS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 85029608089     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.08.044     Document Type: Article

References (66)

1. Atkinson, N., Feike, D., Mackinder, L.C.M., Meyer, M.T., Griffiths, H., Jonikas, M.C., Smith, A.M., McCormick, A.J., Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol. J. 14 (2016), 1302–1315.
2. Atteia, A., Adrait, A., Brugière, S., Tardif, M., van Lis, R., Deusch, O., Dagan, T., Kuhn, L., Gontero, B., Martin, W., et al. A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the α-proteobacterial mitochondrial ancestor. Mol. Biol. Evol. 26 (2009), 1533–1548.
3. 2 concentrating mechanisms. Photosynth. Res. 77 (2003), 83–94.
4. Bauwe, H., Hagemann, M., Fernie, A.R., Photorespiration: players, partners and origin. Trends Plant Sci. 15 (2010), 330–336.
5. Behrends, C., Sowa, M.E., Gygi, S.P., Harper, J.W., Network organization of the human autophagy system. Nature 466 (2010), 68–76.
6. Ben-Shem, A., Frolow, F., Nelson, N., Crystal structure of plant photosystem I. Nature 426 (2003), 630–635.
7. Benlloch, R., Shevela, D., Hainzl, T., Grundström, C., Shutova, T., Messinger, J., Samuelsson, G., Sauer-Eriksson, A.E., Crystal structure and functional characterization of photosystem II-associated carbonic anhydrase CAH3 in Chlamydomonas reinhardtii. Plant Physiol. 167 (2015), 950–962.
8. Bergeron-Sandoval, L.-P., Safaee, N., Michnick, S.W., Mechanisms and consequences of macromolecular phase separation. Cell 165 (2016), 1067–1079.
9. Blanco-Rivero, A., Shutova, T., Román, M.J., Villarejo, A., Martinez, F., Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS ONE, 7, 2012, e49063.
10. 2 deprivation coincides with massive transcriptional restructuring in Chlamydomonas reinhardtii. Plant Cell 24 (2012), 1860–1875.
11. Cameron, J.C., Wilson, S.C., Bernstein, S.L., Kerfeld, C.A., Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155 (2013), 1131–1140.
12. Chevalier, D., Morris, E.R., Walker, J.C., 14-3-3 and FHA domains mediate phosphoprotein interactions. Annu. Rev. Plant Biol. 60 (2009), 67–91.
13. Choi, H.I., Kim, J.Y.H., Kwak, H.S., Sung, Y.J., Sim, S.J., Quantitative analysis of the chemotaxis of a green alga, Chlamydomonas reinhardtii, to bicarbonate using diffusion-based microfluidic device. Biomicrofluidics, 10, 2016, 014121.
14. Cross, F.R., Tying down loose ends in the Chlamydomonas genome: functional significance of abundant upstream open reading frames. G3 (Bethesda) 6 (2016), 435–446.
15. Depège, N., Bellafiore, S., Rochaix, J.-D., Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299 (2003), 1572–1575.
16. Dismukes, G.C., Klimov, V.V., Baranov, S.V., Kozlov, Y.N., DasGupta, J., Tyryshkin, A., The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc. Natl. Acad. Sci. USA 98 (2001), 2170–2175.
17. Elias, J.E., Gygi, S.P., Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4 (2007), 207–214.
18. Emanuelsson, O., Nielsen, H., Brunak, S., von Heijne, G., Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300 (2000), 1005–1016.
19. Engel, B.D., Ishikawa, H., Wemmer, K.A., Geimer, S., Wakabayashi, K., Hirono, M., Craige, B., Pazour, G.J., Witman, G.B., Kamiya, R., Marshall, W.F., The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J. Cell Biol. 199 (2012), 151–167.
20. Engel, B.D., Schaffer, M., Kuhn Cuellar, L., Villa, E., Plitzko, J.M., Baumeister, W., Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife, 4, 2015, e04889.
21. 2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 24 (2012), 1876–1893.
22. Field, C.B., Behrenfeld, M.J., Randerson, J.T., Falkowski, P., Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281 (1998), 237–240.
23. 2-concentrating organelle is liquid like and exhibits dynamic reorganization. Cell 171 (2017), 148–162 this issue.
24. Fuhrmann, M., Oertel, W., Hegemann, P., A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 19 (1999), 353–361.
25. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Hutchison, C.A. 3rd, Smith, H.O., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6 (2009), 343–345.
26. Heinnickel, M., Kim, R.G., Wittkopp, T.M., Yang, W., Walters, K.A., Herbert, S.K., Grossman, A.R., Tetratricopeptide repeat protein protects photosystem I from oxidative disruption during assembly. Proc. Natl. Acad. Sci. USA 113 (2016), 2774–2779.
27. 2-controlled stomatal movements in guard cells. Nat. Cell Biol. 12 (2010), 87–93 1–18.
28. Jansen, R., Greenbaum, D., Gerstein, M., Relating whole-genome expression data with protein-protein interactions. Genome Res. 12 (2002), 37–46.
29. Jin, S., Sun, J., Wunder, T., Tang, D., Cousins, A.B., Sze, S.K., Mueller-Cajar, O., Gao, Y.-G., Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases. Proc. Natl. Acad. Sci. USA 113 (2016), 14716–14721.
30. Johnson, X., Alric, J., Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot. Cell 12 (2013), 776–793.
31. - exchange. J. Physiol. 589 (2011), 1551–1569.
32. Karcher, D., Köster, D., Schadach, A., Klevesath, A., Bock, R., The Chlamydomonas chloroplast HLP protein is required for nucleoid organization and genome maintenance. Mol. Plant 2 (2009), 1223–1232.
33. 2. EMBO J. 17 (1998), 1208–1216.
34. Kobayashi, Y., Takusagawa, M., Harada, N., Fukao, Y., Yamaoka, S., Kohchi, T., Hori, K., Ohta, H., Shikanai, T., Nishimura, Y., Eukaryotic components remodeled chloroplast nucleoid organization during the green plant evolution. Genome Biol. Evol. 8 (2015), 1–16.
35. Kropat, J., Hong-Hermesdorf, A., Casero, D., Ent, P., Castruita, M., Pellegrini, M., Merchant, S.S., Malasarn, D., A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J. 66 (2011), 770–780.
36. Lemeille, S., Willig, A., Depège-Fargeix, N., Delessert, C., Bassi, R., Rochaix, J.D., Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol., 7, 2009, e45.
37. Liu, J., Yang, H., Lu, Q., Wen, X., Chen, F., Peng, L., Zhang, L., Lu, C., PsbP-domain protein1, a nuclear-encoded thylakoid lumenal protein, is essential for photosystem I assembly in Arabidopsis. Plant Cell 24 (2012), 4992–5006.
38. Long, S.P., Marshall-Colon, A., Zhu, X.G., Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161 (2015), 56–66.
39. Lunde, C., Jensen, P.E., Haldrup, A., Knoetzel, J., Scheller, H.V., The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408 (2000), 613–615.
40. Ma, Y., Pollock, S.V., Xiao, Y., Cunnusamy, K., Moroney, J.V., Identification of a novel gene, CIA6, required for normal pyrenoid formation in Chlamydomonas reinhardtii. Plant Physiol. 156 (2011), 884–896.
41. Mackinder, L.C.M., Meyer, M.T., Mettler-Altmann, T., Chen, V.K., Mitchell, M.C., Caspari, O., Freeman Rosenzweig, E.S., Pallesen, L., Reeves, G., Itakura, A., et al. A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle. Proc. Natl. Acad. Sci. USA 113 (2016), 5958–5963.
42. McKay, R.M.L., Gibbs, S.P., Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can. J. Bot. 69 (1991), 1040–1052.
43. Mitra, M., Lato, S.M., Ynalvez, R.A., Xiao, Y., Moroney, J.V., Identification of a new chloroplast carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol. 135 (2004), 173–182.
44. Moroney, J.V., Ma, Y., Frey, W.D., Fusilier, K.A., Pham, T.T., Simms, T.A., DiMario, R.J., Yang, J., Mukherjee, B., The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth. Res. 109 (2011), 133–149.
45. Morris, J.H., Knudsen, G.M., Verschueren, E., Johnson, J.R., Cimermancic, P., Greninger, A.L., Pico, A.R., Affinity purification-mass spectrometry and network analysis to understand protein-protein interactions. Nat. Protoc. 9 (2014), 2539–2554.
46. Neupert, J., Karcher, D., Bock, R., Generation of Chlamydomonas strains that efficiently express nuclear transgenes. Plant J. 57 (2009), 1140–1150.
47. 2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22 (2010), 3105–3117.
48. Pazour, G.J., Agrin, N., Leszyk, J., Witman, G.B., Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170 (2005), 103–113.
49. 2 concentrating mechanism. Plant Physiol. 91 (1989), 505–513.
50. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J. Exp. Bot. 59 (2008), 1441–1461.
51. -. Am. J. Physiol. Cell Physiol. 294 (2008), C1371–C1377.
52. Reinfelder, J.R., Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci. 3 (2011), 291–315.
53. Rochaix, J.-D., Perron, K., Dauvillée, D., Laroche, F., Takahashi, Y., Goldschmidt-Clermont, M., Post-transcriptional steps involved in the assembly of photosystem I in Chlamydomonas. Biochem. Soc. Trans. 32 (2004), 567–570.
54. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
55. Sowa, M.E., Bennett, E.J., Gygi, S.P., Harper, J.W., Defining the human deubiquitinating enzyme interaction landscape. Cell 138 (2009), 389–403.
56. Tardif, M., Atteia, A., Specht, M., Cogne, G., Rolland, N., Brugière, S., Hippler, M., Ferro, M., Bruley, C., Peltier, G., et al. PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol. Biol. Evol. 29 (2012), 3625–3639.
57. Terashima, M., Specht, M., Naumann, B., Hippler, M., Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol. Cell. Proteomics 9 (2010), 1514–1532.
58. Thever, M.D., Saier, M.H. Jr., Bioinformatic characterization of p-type ATPases encoded within the fully sequenced genomes of 26 eukaryotes. J. Membr. Biol. 229 (2009), 115–130.
59. Tresguerres, M., Buck, J., Levin, L.R., Physiological carbon dioxide, bicarbonate, and pH sensing. Pfluegers Arch. 460 (2010), 953–964.
60. 2 limitation induces specific redox-dependent protein phosphorylation in Chlamydomonas reinhardtii. Proteomics 6 (2006), 2693–2704.
61. Updike, D.L., Hachey, S.J., Kreher, J., Strome, S., P granules extend the nuclear pore complex environment in the C. elegans germ line. J. Cell Biol. 192 (2011), 939–948.
62. 2 in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103 (2006), 10110–10115.
63. 2: how Chlamydomonas works against the gradient. Plant J. 82 (2015), 429–448.
64. 2+-binding protein CAS in the green alga Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 113 (2016), 12586–12591.
65. 2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol. 51 (2010), 1453–1468.
66. Yamano, T., Sato, E., Iguchi, H., Fukuda, Y., Fukuzawa, H., Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 112 (2015), 7315–7320.