Evolution of rhodopsin ion pumps in haloarchaea

BackgroundThe 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.ResultsMapping 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.ConclusionThe 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.

[1]  L. Hochstein,et al.  The Biology of HALOPHILIC BACTERIA , 1992 .

[2]  M. Dyall-Smith,et al.  Combined Use of Cultivation-Dependent and Cultivation-Independent Methods Indicates that Members of Most Haloarchaeal Groups in an Australian Crystallizer Pond Are Cultivable , 2004, Applied and Environmental Microbiology.

[3]  Y. Mukohata,et al.  An Australian halobacterium contains a novel proton pump retinal protein: archaerhodopsin. , 1988, Biochemical and biophysical research communications.

[4]  E. Delong,et al.  Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. , 2007, Environmental microbiology.

[5]  Min Pan,et al.  Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. , 2004, Genome research.

[6]  J. Spudich Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsins , 1998, Molecular microbiology.

[7]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[8]  J. Spudich,et al.  Microbial rhodopsins: functional versatility and genetic mobility. , 2006, Trends in microbiology.

[9]  J. Spudich,et al.  Microbial Rhodopsins: Phylogenetic and Functional Diversity , 2005 .

[10]  W. Baumeister,et al.  The Chaperones of the archaeon Thermoplasma acidophilum. , 2001, Journal of structural biology.

[11]  Detection and expression of a gene encoding a new bacteriorhodopsin from an extreme halophile strain HT (JCM 9743) which does not possess bacteriorhodopsin activity , 1998, Extremophiles.

[12]  Olivier Gascuel,et al.  PHYML Online: A Web Server for Fast Maximum Likelihood-Based Phylogenetic Inference , 2018 .

[13]  Frede Thingstad,et al.  Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. , 2002, Environmental microbiology.

[14]  A. Oren Halophilic Microorganisms and their Environments , 2002, Cellular Origin, Life in Extreme Habitats and Astrobiology.

[15]  S. Whelan,et al.  A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. , 2001, Molecular biology and evolution.

[16]  N. Baliga,et al.  Genomic and genetic dissection of an archaeal regulon , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Thompson,et al.  Multiple sequence alignment with Clustal X. , 1998, Trends in biochemical sciences.

[18]  J. Spudich,et al.  Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[19]  David J. Reiss,et al.  Integrated biclustering of heterogeneous genome-wide datasets for the inference of global regulatory networks , 2006, BMC Bioinformatics.

[20]  W. Doolittle,et al.  The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Eric Bapteste,et al.  Evolution of the RNA polymerase B' subunit gene (rpoB') in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. , 2004, Molecular biology and evolution.

[22]  J. Spudich,et al.  Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-transduction mutants of Halobacterium halobium. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Y. Mukohata,et al.  Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. , 1977, Biochemical and biophysical research communications.

[24]  J. Felsenstein Cases in which Parsimony or Compatibility Methods will be Positively Misleading , 1978 .

[25]  E. Delong,et al.  Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea , 2006, Nature.

[26]  Y. Mukohata,et al.  The light-driven proton pump, cruxrhodopsin-2 in Haloarcula sp. arg-2 (bR+, hR-), and its coupled ATP formation. , 1994, Biochimica et biophysica acta.

[27]  Y. Mukohata,et al.  Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. , 1999, Journal of molecular biology.

[28]  W. Baumeister,et al.  The Janus Face of the Archaeal Cdc48/p97 Homologue VAT: Protein Folding versus Unfolding , 1999, Biological chemistry.

[29]  R. Yatsunami,et al.  A novel bacteriorhodopsin-like protein from Haloarcula japonica strain TR-1: gene cloning, sequencing, and transcript analysis , 2000, Extremophiles.

[30]  V. Thorsson,et al.  Genome sequence of Halobacterium species NRC-1. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Winslow R. Briggs,et al.  Handbook of Photosensory Receptors , 2005 .

[32]  W. Doolittle,et al.  Diversity of bacteriorhodopsins in different hypersaline waters from a single Spanish saltern. , 2003, Environmental microbiology.

[33]  D. Bryant,et al.  Prokaryotic photosynthesis and phototrophy illuminated. , 2006, Trends in microbiology.

[34]  S. DasSarma,et al.  brp and blh Are Required for Synthesis of the Retinal Cofactor of Bacteriorhodopsin in Halobacterium salinarum * , 2001, The Journal of Biological Chemistry.

[35]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[36]  N. Kamo,et al.  Evidence that the long-lifetime photointermediate of s-rhodopsin is a receptor for negative phototaxis in Halobacterium halobium. , 1985, Biochemical and biophysical research communications.

[37]  J. Antón,et al.  Xanthorhodopsin: A Proton Pump with a Light-Harvesting Carotenoid Antenna , 2005, Science.

[38]  Y. Mukohata,et al.  Halobacterial rhodopsins. , 1999, Journal of biochemistry.

[39]  Aharon Oren,et al.  Halobacterium sodomense sp. nov., a Dead Sea Halobacterium with an Extremely High Magnesium Requirement , 1983 .

[40]  Henk Bolhuis,et al.  Environmental genomics of "Haloquadratum walsbyi" in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species , 2006, BMC Genomics.

[41]  E V Koonin,et al.  AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. , 1999, Genome research.

[42]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[43]  N. P. Ulrih,et al.  Diversity of halophilic archaea in the crystallizers of an Adriatic solar saltern. , 2005, FEMS microbiology ecology.

[44]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[45]  W. Doolittle,et al.  Frequent Recombination in a Saltern Population of Halorubrum , 2004, Science.

[46]  Friedhelm Pfeiffer,et al.  Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. , 2005, Genome research.

[47]  B. Schobert,et al.  Halorhodopsin is a light-driven chloride pump. , 1982, The Journal of biological chemistry.

[48]  A. von Haeseler,et al.  IQPNNI: moving fast through tree space and stopping in time. , 2004, Molecular biology and evolution.

[49]  Min Pan,et al.  Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  B. Jones,et al.  Halovivax asiaticus gen. nov., sp. nov., a novel extremely halophilic archaeon isolated from Inner Mongolia, China. , 2006, International journal of systematic and evolutionary microbiology.

[51]  J. Imhoff,et al.  Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern , 1985, Microbial Ecology.

[52]  R. M. Martínez-Espinosa,et al.  Respiratory nitrate and nitrite pathway in the denitrifier haloarchaeon Haloferax mediterranei. , 2006, Biochemical Society Transactions.

[53]  Friedhelm Pfeiffer,et al.  The genome of the square archaeon Haloquadratum walsbyi : life at the limits of water activity , 2006, BMC Genomics.

[54]  D Oesterhelt,et al.  Anaerobic growth of halobacteria. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[55]  H. Steinhoff,et al.  Sensory rhodopsin II and bacteriorhodopsin: Light activated helix F movement , 2004, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[56]  W. Doolittle,et al.  Archaeal diversity along a soil salinity gradient prone to disturbance. , 2005, Environmental microbiology.

[57]  J. Spudich,et al.  Deletion mapping of the sites on the HtrI transducer for sensory rhodopsin I interaction , 1996, Journal of bacteriology.

[58]  D. Oesterhelt,et al.  Functions of a new photoreceptor membrane. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Eichler,et al.  Extreme Secretion: Protein Translocation Across the Archaeal Plasma Membrane , 2004, Journal of bioenergetics and biomembranes.