Login | Register

Evolution of rhodopsin ion pumps in haloarchaea


Evolution of rhodopsin ion pumps in haloarchaea

Sharma, Adrian K., Walsh, David A., Bapteste, Eric, Rodriguez-Valera, Francisco, Ford Doolittle, W. and Papke, R Thane (2007) Evolution of rhodopsin ion pumps in haloarchaea. BMC Evolutionary Biology, 7 (1). p. 79. ISSN 14712148

[thumbnail of Walsh_BMCEvolutionaryBiology2007.pdf]
Text (application/pdf)
Walsh_BMCEvolutionaryBiology2007.pdf - Published Version

Official URL: http://dx.doi.org/10.1186/1471-2148-7-79


The type 1 (microbial) rhodopsins are a diverse group of photochemically reactive proteins that display a broad yet patchy distribution among the three domains of life. Recent work indicates that this pattern is likely the result of lateral gene transfer (LGT) of rhodopsin genes between major lineages, and even across domain boundaries. Within the lineage in which the microbial rhodopsins were initially discovered, the haloarchaea, a similar patchy distribution is observed. In this initial study, we assess the roles of LGT and gene loss in the evolution of haloarchaeal rhodopsin ion pump genes, using phylogenetics and comparative genomics approaches.

Mapping presence/absence of rhodopsins onto the phylogeny of the RNA polymerase B' subunit (RpoB') of the haloarchaea supports previous notions that rhodopsins are patchily distributed. The phylogeny for the bacteriorhodopsin (BR) protein revealed two discrepancies in comparison to the RpoB' marker, while the halorhodopsin (HR) tree showed incongruence to both markers. Comparative analyses of bacteriorhodopsin-linked regions of five haloarchaeal genomes supported relationships observed in the BR tree, and also identified two open reading frames (ORFs) that were more frequently linked to the bacteriorhodopsin gene than those genes previously shown to be important to the function and expression of BR.

The evidence presented here reveals a complex evolutionary history for the haloarchaeal rhodopsins, with both LGT and gene loss contributing to the patchy distribution of rhodopsins within this group. Similarities between the BR and RpoB' phylogenies provide supportive evidence for the presence of bacteriorhodopsin in the last common ancestor of haloarchaea. Furthermore, two loci that we have designated bacterio-opsin associated chaperone (bac) and bacterio-opsin associated protein (bap) are inferred to have important roles in BR biogenesis based on frequent linkage and co-transfer with bacteriorhodopsin genes.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Sharma, Adrian K. and Walsh, David A. and Bapteste, Eric and Rodriguez-Valera, Francisco and Ford Doolittle, W. and Papke, R Thane
Journal or Publication:BMC Evolutionary Biology
Digital Object Identifier (DOI):10.1186/1471-2148-7-79
ID Code:7553
Deposited By: Danielle Dennie
Deposited On:10 May 2011 21:07
Last Modified:18 Jan 2018 17:31


1.Rodriguez-Valera F: Introduction to Saline Environments. In The Biology of Halophilic Bacteria. Edited by Vreeland RHHLI. Boca Raton, Fla. , CRC Press; 1993:1-24.

2.Spudich JL: Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsins. Mol Microbiol 1998, 28(6):1051-1058.

3.Mukohata Y, Sugiyama Y, Ihara K, Yoshida M: An Australian halobacterium contains a novel proton pump retinal protein: archaerhodopsin. Biochem Biophys Res Commun 1988, 151(3):1339-1345.

4.Yatsunami R, Kawakami T, Ohtani H, Nakamura S: Transcriptional regulation of cruxrhodopsin gene from extremely halophilic archaeon Haloarcula japonica strain TR-1. Nucleic Acids Symp Ser 1999, 73-74.

5.Hartmann R, Sickinger HD, Oesterhelt D: Anaerobic growth of halobacteria. Proc Natl Acad Sci U S A 1980, 77(7):3821-3825.

6.Spudich JL, Jung KH: Handbook of Photosensory Receptors. 1st edn edition. Edited by Briggs WR, Spudich JL. Wiley-VCH; 2005:pp.1-24.

7.Oesterhelt D, Stoeckenius W: Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A 1973, 70(10):2853-2857.

8.Frigaard NU, Martinez A, Mincer TJ, DeLong EF: Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 2006, 439(7078):847-850.

9.Matsuno-Yagi A, Mukohata Y: Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. Biochem Biophys Res Commun 1977, 78(1):237-243.

10.Spudich EN, Spudich JL: Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-transduction mutants of Halobacterium halobium. Proc Natl Acad Sci U S A 1982, 79(14):4308-4312.

11.Bogomolni RA, Spudich JL: Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci U S A 1982, 79(20):6250-6254.

12.Schobert B, Lanyi JK: Halorhodopsin is a light-driven chloride pump. J Biol Chem 1982, 257(17):10306-10313.

13.Takahashi T, Mochizuki Y, Kamo N, Kobatake Y: Evidence that the long-lifetime photointermediate of s-rhodopsin is a receptor for negative phototaxis in Halobacterium halobium. Biochem Biophys Res Commun 1985, 127(1):99-105.

14.Lanyi JK: Bioenergetics and transport in extreme halophiles. In The biology of halophilic bacteria. Edited by Vreeland RHHLI. Boca Raton, Fla. , CRC Press; 1993.

15.Oren A: Halophilic microorganisms and their environments. Volume 1. Kluwer Academic; 2002:183-185.

16.Kamekura M, Seno Y, Tomioka H: Detection and expression of a gene encoding a new bacteriorhodopsin from an extreme halophile strain HT (JCM 9743) which does not possess bacteriorhodopsin activity. Extremophiles 1998, 2(1):33-39.

17.Grant WD Kamekura, M., McGenity T.J., Ventosa V.: Halobacteriales . In Bergey's Manual of Systematic Bacteriology. Volume 1. Edited by Garrity GM. Bergey's Manual Trust; 2001:294-334.

18.Yatsunami R, Kawakami T, Ohtani H, Nakamura S: A novel bacteriorhodopsin-like protein from Haloarcula japonica strain TR-1: gene cloning, sequencing, and transcript analysis. Extremophiles 2000, 4(2):109-114.

19.Sugiyama Y, Yamada N, Mukohata Y: The light-driven proton pump, cruxrhodopsin-2 in Haloarcula sp. arg-2 (bR+, hR-), and its coupled ATP formation. Biochim Biophys Acta 1994, 1188(3):287-292.

20.Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, Kimura Y, Mukohata Y: Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J Mol Biol 1999, 285(1):163-174.

21.Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez Perez G, Sharma AK, Nesbo CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F: The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A 2005, 102(50):18147-18152.

22.Sharma AK, Spudich JL, Doolittle WF: Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 2006, 14(11):463-469.

23.McCarren J, Delong EF: Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ Microbiol 2007, 9(4):846-858.

24.Walsh DA, Bapteste E, Kamekura M, Doolittle WF: Evolution of the RNA polymerase B' subunit gene (rpoB') in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. Mol Biol Evol 2004, 21(12):2340-2351.

25.Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D: The genome of the square archaeon Haloquadratum walsbyi : life at the limits of water activity. BMC Genomics 2006, 7:169.

26.Walsh DA, Papke RT, Doolittle WF: Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 2005, 7(10):1655-1666.

27.Falb M, Pfeiffer F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D: Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 2005, 15(10):1336-1343.

28.Castillo AM, Gutierrez MC, Kamekura M, Ma Y, Cowan DA, Jones BE, Grant WD, Ventosa A: Halovivax asiaticus gen. nov., sp. nov., a novel extremely halophilic archaeon isolated from Inner Mongolia, China. Int J Syst Evol Microbiol 2006, 56(Pt 4):765-770.

29.Papke RT, Douady CJ, Doolittle WF, Rodriguez-Valera F: Diversity of bacteriorhodopsins in different hypersaline waters from a single Spanish saltern. Environ Microbiol 2003, 5(11):1039-1045.

30.Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, Deutsch EW, Shannon P, Chiu Y, Weng RS, Gan RR, Hung P, Date SV, Marcotte E, Hood L, Ng WV: Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 2004, 14(11):2221-2234.

31.Pasic L, Bartual SG, Ulrih NP, Grabnar M, Velikonja BH: Diversity of halophilic archaea in the crystallizers of an Adriatic solar saltern. FEMS Microbiol Ecol 2005, 54(3):491-498.

32.Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga NS, Thorsson V, Sbrogna J, Swartzell S, Weir D, Hall J, Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP, Angevine CM, Dale H, Isenbarger TA, Peck RF, Pohlschroder M, Spudich JL, Jung KW, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omer AD, Ebhardt H, Lowe TM, Liang P, Riley M, Hood L, DasSarma S: Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A 2000, 97(22):12176-12181.

33.Baliga NS, Kennedy SP, Ng WV, Hood L, DasSarma S: Genomic and genetic dissection of an archaeal regulon. Proc Natl Acad Sci U S A 2001, 98(5):2521-2525.

34.Peck RF, Echavarri-Erasun C, Johnson EA, Ng WV, Kennedy SP, Hood L, DasSarma S, Krebs MP: brp and blh are required for synthesis of the retinal cofactor of bacteriorhodopsin in Halobacterium salinarum. J Biol Chem 2001, 276(8):5739-5744.

35.Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML: Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 2004, 70(9):5258-5265.

36.Reiss DJ, Baliga NS, Bonneau R: Integrated biclustering of heterogeneous genome-wide datasets for the inference of global regulatory networks. BMC Bioinformatics 2006, 7:280.

37.Baliga NS, Pan M, Goo YA, Yi EC, Goodlett DR, Dimitrov K, Shannon P, Aebersold R, Ng WV, Hood L: Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach. Proc Natl Acad Sci U S A 2002, 99(23):14913-14918.

38.Sonnhammer EL, von Heijne G, Krogh A: A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998, 6:175-182.

39.Krogh A, Larsson B, von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580.

40.3D position specific scoring matrix fold recognition server [http://www.sbg.bio.ic.ac.uk/~3dpssm/]

41.Neuwald AF, Aravind L, Spouge JL, Koonin EV: AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 1999, 9(1):27-43.

42.Felsenstein J: Cases in which parsimony or compatibility methods will be positvely misleading. Systematic Zoology 1978, 27:401-410.

43.Oren A: Halobacterium sodomense sp. nov., a Dead Sea Halobacterium with an extremely high magnesium requirement. Int J Syst Bacteriol 1983, 33:381 -3386.

44.Benlloch S, Lopez-Lopez A, Casamayor EO, Ovreas L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedros-Alio C, Rodriguez-Valera F: Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 2002, 4(6):349-360.

45.F. Rodriguez-Valera AV G. Juez1 and J. F. Imhoff: Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern . Microb Ecol 1985, 11(2):107-115.

46.Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK: Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 2005, 309(5743):2061-2064.

47.Mukohata Y, Ihara K, Tamura T, Sugiyama Y: Halobacterial rhodopsins. J Biochem (Tokyo) 1999, 125(4):649-657.

48.TIGR homepage [http://www.TIGR.org]

49.Martinez-Espinosa RM, Richardson DJ, Butt JN, Bonete MJ: Respiratory nitrate and nitrite pathway in the denitrifier haloarchaeon Haloferax mediterranei. Biochem Soc Trans 2006, 34(Pt 1):115-117.

50.Golbik R, Lupas AN, Koretke KK, Baumeister W, Peters J: The Janus face of the archaeal Cdc48/p97 homologue VAT: protein folding versus unfolding. Biol Chem 1999, 380(9):1049-1062.

51.Ruepp A, Rockel B, Gutsche I, Baumeister W, Lupas AN: The Chaperones of the archaeon Thermoplasma acidophilum. J Struct Biol 2001, 135(2):126-138.

52.Ring G, Eichler J: Extreme secretion: protein translocation across the archael plasma membrane. J Bioenerg Biomembr 2004, 36(1):35-45.

53.Klare JP, Bordignon E, Engelhard M, Steinhoff HJ: Sensory rhodopsin II and bacteriorhodopsin: light activated helix F movement. Photochem Photobiol Sci 2004, 3(6):543-547.

54.Perazzona B, Spudich EN, Spudich JL: Deletion mapping of the sites on the HtrI transducer for sensory rhodopsin I interaction. J Bacteriol 1996, 178(22):6475-6478.

55.Bryant DA, Frigaard NU: Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 2006, 14(11):488-496.

56.Legault BA, Lopez-Lopez A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodriguez-Valera F, Papke RT: Environmental genomics of "Haloquadratum walsbyi" in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 2006, 7:171.

57.NCBI homepage [http://www.ncbi.nlm.nih.gov]

58.Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ: Multiple sequence alignment with Clustal X. Trends Biochem Sci 1998, 23(10):403-405.

59.Maddison DR Maddison, W.P.: MacClade 4: Analysis of Phylogeny and Character Evolution. Sunderland, MA , Sinauer; 2000.

60.Vinh le S, Von Haeseler A: IQPNNI: moving fast through tree space and stopping in time. Mol Biol Evol 2004, 21(8):1565-1571.

61.Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 18(5):691-699.

62.Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.

63.Guindon S, Lethiec F, Duroux P, Gascuel O: PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 2005, 33(Web Server issue):W557-9.

64.Papke RT, Koenig JE, Rodriguez-Valera F, Doolittle WF: Frequent recombination in a saltern population of Halorubrum. Science 2004, 306(5703):1928-1929.

65.Wilson K: Current Protocols In Molecular Biology. Volume 1. Edited by Ausubel FBRKRMDSJSJSK. Canada , John Wiley & Sons, Inc.; 1994.

66.Softberry homepage [http://www.softberry.com]
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page

Downloads per month over past year

Research related to the current document (at the CORE website)
- Research related to the current document (at the CORE website)
Back to top Back to top