1887

Abstract

Chemotaxis allows bacteria to sense gradients in their environment and respond by directing their swimming. Aer is a receptor that, instead of responding to a specific chemoattractant, allows bacteria to sense cellular energy levels and move towards favourable environments. In the number of apparent Aer homologues differs between the only two species it has been characterized in, and . Here we combined bioinformatic approaches with deletional mutagenesis in KF707 to further characterize Aer. It was determined that the number of Aer homologues varies between zero and four throughout the genus , and they were phylogenetically classified into five subgroups. We also used sequence analysis to show that these homologous receptors differ in their HAMP signal transduction domains. Genetic analysis also indicated that some Aer homologues have likely been subject to horizontal transfer. KF707 was unique among strains for having three Aer homologues as well as the receptors CttP and McpB. Phenotypic characterization in this strain showed that the most prevalent homologue of Aer was key, but not essential, for energy taxis. This study demonstrates that energy taxis in varies between species and provides a new naming convention and associated phylogenetic details for Aer chemoreceptors.

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/content/journal/micro/10.1099/mic.0.000864
2019-10-22
2019-11-12
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References

  1. Wadhams GH, Armitage JP. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 2004;5: 1024– 1037 [CrossRef]
    [Google Scholar]
  2. Sampedro I, Parales RE, Krell T, Hill JE. Pseudomonas chemotaxis. FEMS Microbiol Rev 2015;39: 17– 46 [CrossRef]
    [Google Scholar]
  3. Krell T. Tackling the bottleneck in bacterial signal transduction research: high-throughput identification of signal molecules. Mol Microbiol 2015;96: 685– 688 [CrossRef]
    [Google Scholar]
  4. Alexandre G, Greer-Phillips S, Zhulin IB. Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev 2004;28: 113– 126 [CrossRef]
    [Google Scholar]
  5. Bibikov SI, Biran R, Rudd KE, Parkinson JS. A signal transducer for aerotaxis in Escherichia coli. J Bacteriol 1997;179: 4075– 4079 [CrossRef]
    [Google Scholar]
  6. Rebbapragada A, Johnson MS, Harding GP, Zuccarelli AJ, Fletcher HM et al. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Natl Acad Sci USA 1997;94: 10541– 10546 [CrossRef]
    [Google Scholar]
  7. Samanta D, Widom J, Borbat PP, Freed JH, Crane BR. Bacterial energy sensor Aer modulates the activity of the chemotaxis kinase CheA based on the redox state of the flavin cofactor. J Biol Chem 2016;291: 25809– 25814 [CrossRef]
    [Google Scholar]
  8. Hong CS, Shitashiro M, Kuroda A, Ikeda T, Takiguchi N et al. Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa. FEMS Microbiol Lett 2004;231: 247– 252 [CrossRef]
    [Google Scholar]
  9. Watts KJ, Taylor BL, Johnson MS. PAS/poly-HAMP signalling in Aer-2, a soluble haem-based sensor. Mol Microbiol 2011;79: 686– 699 [CrossRef]
    [Google Scholar]
  10. Sarand I, Österberg S, Holmqvist S, Holmfeldt P, Skärfstad E et al. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environ Microbiol 2008;10: 1320– 1334 [CrossRef]
    [Google Scholar]
  11. Garcia D, Watts KJ, Johnson MS, Taylor BL. Delineating PAS-HAMP interaction surfaces and signalling-associated changes in the aerotaxis receptor Aer. Mol Microbiol 2016;100: 156– 172 [CrossRef]
    [Google Scholar]
  12. Garcia D, Orillard E, Johnson MS, Watts KJ. Gas sensing and signaling in the PAS-Heme domain of the Pseudomonas aeruginosa Aer2 receptor. J Bacteriol 2017;199: e00003– 00017 [CrossRef]
    [Google Scholar]
  13. Güvener ZT, Tifrea DF, Harwood CS. Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 2006;61: 106– 118 [CrossRef]
    [Google Scholar]
  14. Nichols NN, Harwood CS. An aerotaxis transducer gene from Pseudomonas putida. FEMS Microbiol Lett 2000;182: 177– 183 [CrossRef]
    [Google Scholar]
  15. Luu RA, Schneider BJ, Ho CC, Nesteryuk V, Ngwesse SE et al. Taxis of Pseudomonas putida F1 toward phenylacetic acid is mediated by the energy taxis receptor Aer2. Appl Environ Microbiol 2013;79: 2416– 2423 [CrossRef]
    [Google Scholar]
  16. Bodilis J, Nsigue Meilo S, Cornelis P, De Vos P, Barray S. A long-branch attraction artifact reveals an adaptive radiation in Pseudomonas. Mol Biol Evol 2011;28: 2723– 2726 [CrossRef]
    [Google Scholar]
  17. Gomila M, Peña A, Mulet M, Lalucat J, García-Valdés E. Phylogenomics and systematics in Pseudomonas. Front Microbiol 2015;6: 214 [CrossRef]
    [Google Scholar]
  18. Fedi S, Barberi TT, Nappi MR, Sandri F, Booth S et al. The role of cheA genes in swarming and swimming motility of Pseudomonas pseudoalcaligenes KF707. Microbes Environ 2016;31: 169– 172 [CrossRef]
    [Google Scholar]
  19. Shitashiro M, Tanaka H, Hong CS, Kuroda A, Takiguchi N et al. Identification of chemosensory proteins for trichloroethylene in Pseudomonas aeruginosa. J Biosci Bioeng 2005;99: 396– 402 [CrossRef]
    [Google Scholar]
  20. Pham HT, Parkinson JS. Phenol sensing by Escherichia coli chemoreceptors: a nonclassical mechanism. J Bacteriol 2011;193: 6597– 6604 [CrossRef]
    [Google Scholar]
  21. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215: 403– 410 [CrossRef]
    [Google Scholar]
  22. Papadopoulos JS, Agarwala R. Cobalt: constraint-based alignment tool for multiple protein sequences. Bioinformatics 2007;23: 1073– 1079 [CrossRef]
    [Google Scholar]
  23. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52: 696– 704 [CrossRef]
    [Google Scholar]
  24. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010;59: 307– 321 [CrossRef]
    [Google Scholar]
  25. Williams KP, Gillespie JJ, Sobral BWS, Nordberg EK, Snyder EE et al. Phylogeny of Gammaproteobacteria. J Bacteriol 2010;192: 2305– 2314 [CrossRef]
    [Google Scholar]
  26. Brandt BW, Feenstra KA, Heringa J. Multi-Harmony: detecting functional specificity from sequence alignment. Nucleic Acids Res 2010;38: W35– W40 [CrossRef]
    [Google Scholar]
  27. Özen AI, Ussery DW. Defining the Pseudomonas genus: where do we draw the line with Azotobacter?. Microb Ecol 2012;63: 239– 248 [CrossRef]
    [Google Scholar]
  28. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P. Smart: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 2000;28: 231– 234 [CrossRef]
    [Google Scholar]
  29. Airola MV, Watts KJ, Crane BR. Identifying divergent HAMP domains and poly-HAMP chains. J Biol Chem 2010;285: le7 [CrossRef]
    [Google Scholar]
  30. Alexander RP, Zhulin IB. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci USA 2007;104: 2885– 2890 [CrossRef]
    [Google Scholar]
  31. Dunin-Horkawicz S, Lupas AN. Comprehensive analysis of HAMP domains: implications for transmembrane signal transduction. J Mol Biol 2010;397: 1156– 1174 [CrossRef]
    [Google Scholar]
  32. Zimmermann L, Stephens A, Nam SZ, Rau D, Kübler J et al. A completely Reimplemented Mpi bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 2018;430: 2237– 2243 [CrossRef]
    [Google Scholar]
  33. Jones DT. Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 1999
    [Google Scholar]
  34. Hmelo LR, Borlee BR, Almblad H, Love ME, Randall TE et al. Precision-engineering the Pseudomonas aeruginosa genome with two-step allelic exchange. Nat Protoc 2015;10: 1820– 1841 [CrossRef]
    [Google Scholar]
  35. Alvarez-Ortega C, Harwood CS. Identification of a malate chemoreceptor in Pseudomonas aeruginosa by screening for chemotaxis defects in an energy taxis-deficient mutant. Appl Environ Microbiol 2007;73: 7793– 7795 [CrossRef]
    [Google Scholar]
  36. Tremaroli V, Fedi S, Tamburini S, Viti C, Tatti E et al. A histidine-kinase cheA gene of Pseudomonas pseudoalcaligens KF707 not only has a key role in chemotaxis but also affects biofilm formation and cell metabolism. Biofouling 2011;27: 33– 46 [CrossRef]
    [Google Scholar]
  37. Nichols NN, Harwood CS. An aerotaxis transducer gene from Pseudomonas putida. FEMS Microbiol Lett 2000;182: 177– 183 [CrossRef]
    [Google Scholar]
  38. Sarand I, Österberg S, Holmqvist S, Holmfeldt P, Skärfstad E et al. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environ Microbiol 2008;10: 1320– 1334 [CrossRef]
    [Google Scholar]
  39. Luu RA, Schneider BJ, Ho CC, Nesteryuk V, Ngwesse SE et al. Taxis of Pseudomonas putida F1 toward phenylacetic acid is mediated by the energy taxis receptor Aer2. Appl Environ Microbiol 2013;79: 2416– 2423 [CrossRef]
    [Google Scholar]
  40. García-Fontana C, Corral Lugo A, Krell T. Specificity of the CheR2 methyltransferase in Pseudomonas aeruginosa is directed by a C-terminal pentapeptide in the McpB chemoreceptor. Sci Signal 2014;7: ra34 [CrossRef]
    [Google Scholar]
  41. Henry JT, Crosson S. Ligand-Binding PAS domains in a genomic, cellular, and structural context. Annu Rev Microbiol 2011;65: 261– 286 [CrossRef]
    [Google Scholar]
  42. Taylor BL. Aer on the inside looking out: paradigm for a PAS-HAMP role in sensing oxygen, redox and energy. Mol Microbiol 2007;65: 1415– 1424 [CrossRef]
    [Google Scholar]
  43. Watts KJ, Ma Q, Johnson MS, Taylor BL. Interactions between the PAS and HAMP domains of the Escherichia coli aerotaxis receptor Aer. J Bacteriol 2004;186: 7440– 7449 [CrossRef]
    [Google Scholar]
  44. Behrens W, Schweinitzer T, McMurry JL, Loewen PC, Buettner FFR et al. Localisation and protein-protein interactions of the Helicobacter pylori taxis sensor TlpD and their connection to metabolic functions. Sci Rep 2016;6: 23582 [CrossRef]
    [Google Scholar]
  45. Pei J, Mitchell DA, Dixon JE, Grishin NV. Expansion of type II CAAX proteases reveals evolutionary origin of γ-secretase subunit APH-1. J Mol Biol 2011;410: 18– 26 [CrossRef]
    [Google Scholar]
  46. Nishiyama SI, Ohno S, Ohta N, Inoue Y, Fukuoka H et al. Thermosensing function of the Escherichia coli redox sensor Aer. J Bacteriol 2010;192: 1740– 1743 [CrossRef]
    [Google Scholar]
  47. Yang Y, Sourjik V. Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis. Mol Microbiol 2012;86: 1482– 1489 [CrossRef]
    [Google Scholar]
  48. Ortega DR, Fleetwood AD, Krell T, Harwood CS, Jensen GJ et al. Assigning chemoreceptors to chemosensory pathways in Pseudomonas aeruginosa. Proc Natl Acad Sci 2017; 201708842
    [Google Scholar]
  49. Bardy SL, Briegel A, Rainville S, Krell T. Recent advances and future prospects in bacterial and archaeal locomotion and signal transduction. J Bacteriol 2017;199: e00203– 00217 [CrossRef]
    [Google Scholar]
  50. Österberg S, Åberg A, Herrera Seitz MK, Wolf-Watz M, Shingler V. Genetic dissection of a motility-associated c-di-GMP signalling protein of Pseudomonas putida. Environ Microbiol Rep 2013;5: 556– 565 [CrossRef]
    [Google Scholar]
  51. Xu L, Xin L, Zeng Y, Yam JKH, Ding Y et al. A cyclic di-GMP-binding adaptor protein interacts with a chemotaxis methyltransferase to control flagellar motor switching. Sci Signal 2016;9: ra102 [CrossRef]
    [Google Scholar]
  52. Zhulin IB. The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv Microb Physiol 2001;45: 157– 198
    [Google Scholar]
  53. Borziak K, Fleetwood AD, Zhulin IB. Chemoreceptor gene loss and acquisition via horizontal gene transfer in Escherichia coli. J Bacteriol 2013;195: 3596– 3602 [CrossRef]
    [Google Scholar]
  54. Qiu X, Kulasekara BR, Lory S. Role of horizontal gene transfer in the evolution of Pseudomonas aeruginosa virulence. Genome Dyn 2009;6: 126– 139 [CrossRef]
    [Google Scholar]
  55. Sengeløv G, Kristensen KJ, Sørensen AH, Kroer N, Sørensen SJ. Effect of genomic location on horizontal transfer of a recombinant gene cassette between Pseudomonas strains in the rhizosphere and spermosphere of barley seedlings. Curr Microbiol 2001;42: 160– 167 [CrossRef]
    [Google Scholar]
  56. Tremaroli V, Vacchi Suzzi C, Fedi S, Ceri H, Zannoni D et al. Tolerance of Pseudomonas pseudoalcaligenes KF707 to metals, polychlorobiphenyls and chlorobenzoates: effects on chemotaxis-, biofilm- and planktonic-grown cells. FEMS Microbiol Ecol 2010;74: 291– 301 [CrossRef]
    [Google Scholar]
  57. Yao J, Allen C. The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J Bacteriol 2007;189: 6415– 6424 [CrossRef]
    [Google Scholar]
  58. Boin MA, Häse CC. Characterization of Vibrio cholerae aerotaxis. FEMS Microbiol Lett 2007;276: 193– 201 [CrossRef]
    [Google Scholar]
  59. Ferrández A, Hawkins AC, Summerfield DT, Harwood CS. Cluster II Che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J Bacteriol 2002;184: 4374– 4383 [CrossRef]
    [Google Scholar]
  60. Kim HE, Shitashiro M, Kuroda A, Takiguchi N, Ohtake H et al. Identification and characterization of the chemotactic transducer in Pseudomonas aeruginosa PAO1 for positive chemotaxis to trichloroethylene. J Bacteriol 2006;188: 6700– 6702 [CrossRef]
    [Google Scholar]
  61. Ortega DR, Subramanian P, Mann P, Kjær A, Chen S et al. Repurposing a macromolecular machine: architecture and evolution of the F7 chemosensory system. bioRxiv 2019; 653600
    [Google Scholar]
  62. Tatusova T, Ciufo S, Fedorov B, O'Neill K, Tolstoy I. Refseq microbial genomes database: new representation and annotation strategy. Nucleic Acids Res 2014;42: D553– D559 [CrossRef]
    [Google Scholar]
  63. Cochrane G, Karsch-Mizrachi I, Takagi T. International Nucleotide Sequence Database Collaboration The International nucleotide sequence database collaboration. Nucleic Acids Res 2016;44: D48– D50 [CrossRef]
    [Google Scholar]
  64. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009;25: 1189– 1191 [CrossRef]
    [Google Scholar]
  65. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32: 1792– 1797 [CrossRef]
    [Google Scholar]
  66. R Core Team R: A language and environment for statistical computing. R Found Stat Comput Vienna, Austria 2014;2014:
    [Google Scholar]
  67. Wickham H. ggplot2. WIREs Comp Stat 2011;3: 180– 185 [CrossRef]
    [Google Scholar]
  68. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F et al. Cdd: NCBI's conserved domain database. Nucleic Acids Res 2015;43: D222– D226 [CrossRef]
    [Google Scholar]
  69. Crooks GE, Hon G, Chandonia JM, Brenner SE. Weblogo: a sequence logo generator. Genome Res 2004;14: 1188– 1190 [CrossRef]
    [Google Scholar]
  70. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013;30: 772– 780 [CrossRef]
    [Google Scholar]
  71. Deng W, Maust BS, Nickle DC, Learn GH, Liu Y et al. DIVEIN: a web server to analyze phylogenies, sequence divergence, diversity, and informative sites. Biotechniques 2010;48: 405– 408 [CrossRef]
    [Google Scholar]
  72. Huson DH, Scornavacca C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol 2012;61: 1061– 1067 [CrossRef]
    [Google Scholar]
  73. Maseda H, Sawada I, Saito K, Uchiyama H, Nakae T et al. Enhancement of the mexAB-oprM efflux pump expression by a quorum-sensing autoinducer and its cancellation by a regulator, MexT, of the mexEF-oprN efflux pump operon in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2004;48: 1320– 1328 [CrossRef]
    [Google Scholar]
  74. Triscari-Barberi T, Simone D, Calabrese FM, Attimonelli M, Hahn KR et al. Genome sequence of the polychlorinated-biphenyl degrader Pseudomonas pseudoalcaligenes KF707. J Bacteriol 2012;194: 4426– 4427 [CrossRef]
    [Google Scholar]
  75. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: A laboratory manual. Volumes 1, 2, and 3. Current protocols in molecular biology. Volumes 1 and 2, 2nd ed. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 1989
    [Google Scholar]
  76. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012;13: 134 [CrossRef]
    [Google Scholar]
  77. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 1979;76: 1648– 1652 [CrossRef]
    [Google Scholar]
  78. Schneider CA, Rasband WS, Eliceiri KW. Nih image to ImageJ: 25 years of image analysis. Nat Methods 2012;9: 671– 675 [CrossRef]
    [Google Scholar]
  79. Silva-Rocha R, Martínez-García E, Calles B, Chavarría M, Arce-Rodríguez A et al. The standard European vector architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res 2013;41: D666– D675 [CrossRef]
    [Google Scholar]
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