Light-promoted rhodopsin expression and starvation survival in the marine dinoflagellate Oxyrrhis marina

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Guo, Zhiling ^a,b,e   Zhang, Huan ^a,c   Lin, Senjie ^a,d  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^c OCEAN UNIVERSITY OF CHINA   (China)

^d XIAMEN UNIVERSITY   (China)

^e RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; RHODOPSIN; PROTOZOAL PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DINOFLAGELLATE; EUKARYOTE; GENE AMPLIFICATION; GENE SILENCING; GENETIC TRANSCRIPTION; GROWTH RATE; HIGH THROUGHPUT SEQUENCING; IN VITRO STUDY; LIGHT DARK CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYRRHIS MARINA; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; AMINO ACID SEQUENCE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; MOLECULAR GENETICS; PHYSIOLOGY; STARVATION;

DINOPHYCEAE; EUKARYOTA; OXYRRHIS MARINA; PROTEOBACTERIA;

AMINO ACID SEQUENCE; DINOFLAGELLIDA; GENE EXPRESSION REGULATION; LIGHT; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; RHODOPSIN; STARVATION; TRANSCRIPTOME;

EID: 84918517158     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114941     Document Type: Article

References (67)

1. Béjà O (2000) Bacterial Rhodopsin:Evidence for a new type of phototrophy in the sea. Science 289: 1902-1906.
2. Fuhrman JA, Schwalbach MS, Stingl U (2008) Proteorhodopsins an array of physiological roles. Nat Rev Microbiol 6: 488-494.
3. Kikukawa T, Tamogami J, Shimono K, Demura M, Nara T, et al. (2012) Photo-induced Proton Transfers of Microbial Rhodopsins. In: Rijeka, Croatia, Saha S, editors. Molecular photochemistry-Various aspects. In Tech. pp 89-108.
4. Litmann BJ, Mitchell DC (1996) Rhodopsin structure and function. In: Greenwich, Lee AG, editors. Rhodopsin and G-Protein Linked Receptors, Part A. In JAI Press. pp 1-32.
5. Ruiz-Gonzalez MX, Marin I (2004) New insights into the evolutionary history of type 1 rhodopsins. J Mol Evol 58: 348-358.
6. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19: 385-419.
7. Bieszke JA, Braun EL, Bean LE, Kang S, Natvig DO, et al. (1999) The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. Proc Natl Acad Sci USA 96: 8034-8039.
8. Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of halobacterium halobium. Nat New Biol 233: 149-152.
9. Englander JJ, Englander SW (1977) Comparison of bacterial and animal rhodopsins by hydrogen. Nature 265(5595): 658-659.
10. Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins:functional versatility and genetic mobility. Trends Microbiol 14: 463-469.
11. Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature 411: 786-789.
12. Schobert B, Lanyi JK (1982) Halorhodopsin is a light-driven chloride pump. J Biol Chem 257: 10306-10313.
13. Bogomolni RA, Spudich JL (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci USA 79: 6250-6254.
14. Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, et al. (1999) Evolution of the archaeal rhodopsins:evolution rate changes by gene duplication and functional differentiation. J Mol Biol 285: 163-174.
15. Tomioka H, Takahashi T, Kamo N, Kobatake Y (1986) Flash spectrophotometric identification of a fourth rhodopsin-like pigment in Halobacterium halobium. Biochem Biophys Res Commun 139: 389-395.
16. 2. Pharmaceut Res 14: 1533-1541.
17. Idnurm A, Howlett BJ (2001) Characterization of an opsin gene from the ascomycete Leptosphaeria maculans. Genome 44: 167-171.
18. Waschuk SA, Bezerra AG, Shi L, Brown LS (2005) Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci USA 102: 6879-6883.
19. Yutin N, Koonin EV (2012) Proteorhodopsin genes in giant viruses. Yutin Koonin Biol Direct 7: 34
20. Finkel OM, Beja O, Belkin S (2013) Global abundance of microbial rhodopsins. ISME J. 7: 448-451.
21. Balashov SP, Imasheva ES, Boichenko VA, Antón J, Wang JM, et al. (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309: 2061-2064.
22. Atamna-Ismaeel N, Finkel OM, Glaser F, Sharon I, Schneider R, et al. (2012) Microbial rhodopsins on leave surfaces of terrestrial plants. Environ Microbiol 14: 140-146.
23. Spudich JL, Yang C, Jung K-H, Spudich EN (2000.) Retinylidene proteins structures and functions from archaea to humans. Annu Rev Cell Dev Biol 16: 365-392.
24. Martinez A, Bradley AS, Waldbauer JR, Summons RE, DeLong EF (2007) Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc Natl Acad Sci USA 104: 5590-5595.
25. Walter JM, Greenfield D, Bustamante C, Liphardt J (2007) Light-powering Escherichia coli with proteorhodopsin. Proc Natl Acad Sci USA 104: 2408-2412.
26. Balashov SP, Lanyi JK (2007) Xanthorhodopsin: Proton pump with a carotenoid antenna. Cell Mol Life Sci 64: 2323-2328.
27. Mongodin EF, Nelson K, Daugherty S, Deboy R, Wister J, et al. (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102: 18147-18152.
28. Hoff WD, Jung KH, Spudich JL (1997) Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu Rev Biophys Biomol Struct 26: 223-258.
29. Kunio I, Tohru U, Izumi K, Tomomi K-I, Yasuo S, et al. (1999) Evolution of the archaeal rhodopsins evolution rate changes by gene duplication and functional differentiation. J Mol Biol 285: 163-174.
30. Frassanito AM, Barsanti L, Passarelli V, Evangelista V, Gualtieri P (2010) A rhodopsin-like protein in Cyanophora paradoxa:gene sequence and protein immunolocalization. Cell Mol Life Sci 67: 965-971.
31. Gualtieri P, Pelosi P, Passarelli V, Barsanti L (1992) Identification of a rhodopsin photoreceptor in Euglena gracilis. Biochim Biophys Acta 1117: 55-59.
32. Laura B, Vincenzo P, Paola L, Patricial W, Dunlap JR, et al. (1993) Effects of hydroxylamine digitonin and triton X-100 on photoreceptor (paraflagellar swelling) and photoreception of Euglena gracilis. Vision Res 33: 2043-2050.
33. Lin S, Zhang H, Zhuang Y, Tran B, Gill J (2010) Spliced leader-based metatranscriptomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc Natl Acad Sci USA 107: 20033-20038.
34. Sineshchekov OA, Govorunova EG, Jung KH, Zauner S, Maier UG, et al. (2005) Rhodopsin-mediated photoreception in cryptophyte flagellates. Biophys J 89: 4310-4319.
35. +-pumping rhodopsin from the marine alga Acetabularia. Biophys J 91: 1471-1479.
36. Georg N, Doris O, Markus F, Suneel K, Anna MM, et al. (2002) Channelrhodopsin-1 a light-gated proton channel in green algae. Science, New Series 296: 2395-2398.
37. Sineshchekov OA, Jung KH, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99: 8689-8694.
38. Zhang H, Hou Y, Miranda L, Campbell DA, Sturm NR, et al. (2007) Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci USA 104: 4618-4623.
39. Slamovits CH, Okamoto N, Burri L, James ER, Keeling PJ (2011) A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat Commun 2: 1-6.
40. Lowe CD, Keeling PJ, Martin LE, Slamovits CH, Watts PC, et al. (2010) Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. J Plankton Res 33: 555-567.
41. Slamovits CH, Keeling PJ (2010) Contributions of Oxyrrhis marina to molecular biology, genomics and organelle evolution of dinoflagellates. J Plankton Res 33: 591-602.
42. Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010) Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveolata:Dinophyceae). Protist 161: 212-221.
43. Guo ZL, Zhang H, Liu S, Lin S (2013) Biology of the marine heterotrophic dinoflagellate Oxyrrhis marina:current status and future directions. Microorganisms 1: 33-57.
44. Hartz AJ, Sherr BF, Sherr EB (2011) Photoresponse in the heterotrophic marine dinoflagellate Oxyrrhis marina. J Eukaryot Microbiol 58: 171-177.
45. Zhang H, Finiguerra M, Dam HG, Huang Y, Xu D, et al. (2013) An improved method for achieving high-quality RNA for copepod transcriptomic studies. J Exp Mar Biol Ecol 446: 57-66.
46. Moreno-Paz M, Parro V (2006) Amplification of low quantity bacterial RNA for microarray studies: time-course analysis of Leptospirillum ferrooxidans under nitrogen-fixing conditions. Environ Microbiol 8: 1064-1073.
47. th International Conference on Harmful Alge, International Society for the Study of Harmful Algae, pp. 166-170.
48. Zhang H, Zhuang Y, Gill J, Lin S (2013) Proof that dinoflagellate spliced leader (DinoSL) is a useful hook for fishing dinoflagellate transcripts from mixed microbial samples: Symbiodinium kawagutii as a case study. Protist 164: 510-527.
49. Lin X, Zhang H, Huang B, Lin S (2011) Alkaline phosphatase gene sequence and transcriptional regulation by phosphate limitation in Amphidinium carterae (Dinophyceae). J Phycol 47: 1110-1120.
50. Thompson JD, Higgins GD, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gappenalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
51. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
52. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
53. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
54. Zhang H, Hou Y, Lin S (2006) Isolation and characterization of proliferating cell nuclear antigen from the dinoflagellate Pfiesteria piscicida. J Eukaryot Microbiol 53: 142-150.
55. Zhang H, Zhuang Y, Gill J, Lin S (2013) Proof that dinoflagellate spliced leader (DinoSL) is a useful hook for fishing dinoflagellate transcripts from mixed microbial samples: Symbiodinium kawagutii as a case study. Protist 164: 510-527.
56. Gomez-Consarnau L, Gonzalez JM, Coll-Llado M, Gourdon P, Pascher T, et al. (2007) Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445: 210-213.
57. Wang Z, O'Shaughnessy TJ, Soto CM, Rahbar AM, Robertson KL, et al. (2012) Function and regulation of Vibrio campbellii proteorhodopsin: acquired phototrophy in a classical organoheterotroph. PLoS ONE 7: 1-8.
58. Jeong HJ, Seong KA, Yoo YD, Kim TH, Kang NS, et al. (2008) Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. J Eukaryot Microbiol 55: 271-288.
59. Skovgaard A (1996) Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar Ecol Prog Ser 143: 247-253.
60. Caron DA, Sanders RW, Lim EL, Marrasé C, Amaral L, et al. (1993) Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum. Microb Ecol 25: 93-111.
61. Li A, Stoecker DK, Coats DW (2000) Mixotrophy in Gyrodinium galatheanum (DINOPHYCEAE): grazing responses to light intensity and inorganic nutrients. J Phycol 36: 33-45.
62. Feinstein TN, Traslavina R, Sun M, Lin S (2002) Effects of light on photosynthesis, grazing, and population dynamics of the heterotrophic dinoflagellate Pfiesteria Piscicida (Dinophyceae). J Phycol 38: 659-669.
63. Gomez-Consarnau L, Akram N, Lindell K, Pedersen A, Neutze R, et al. (2010) Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol 8: 1-10.
64. Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, et al. (2011) Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci USA 109: E317-E325.
65. Feng S, Powell SM, Wilson R, Bowman JP (2013). Light-stimulated growth of proteorhodopsin-bearing sea-ice psychrophile Psychroflexus torquis is salinity dependent. ISME J 7: 2206-2213.
66. Kuo RC, Zhang H, Zhuang Y, Hannick L, Lin S (2013) Transcriptomic study reveals widespread spliced leader trans-splicing, short 5′-UTRs and potential complex carbon fixation mechanisms in the euglenoid Alga Eutreptiella sp. PLoS One 8: 1-12.
67. Zhang H, Bhattacharya D, Lin S (2005) Phylogeny of Dinoflagellates Based on Mitochondrial Cytochrome B and Nuclear Small Subunit Rdna Sequence Comparisons. J Phycol 41: 411-420.