1887

Abstract

Bacteria have evolved the ability to monitor changes in various physico-chemical parameters and to adapt their physiology and metabolism by implementing appropriate cellular responses to these changes. Energy taxis is a metabolism-dependent form of taxis and is the directed movement of motile bacteria in gradients of physico-chemical parameters that affect metabolism. Energy taxis has been described in diverse bacterial species and several dedicated energy sensors have been identified. The molecular mechanism of energy taxis has not been studied in as much detail as chemotaxis, but experimental evidence indicates that this behaviour differs from metabolism-independent taxis only by the presence of dedicated energy taxis receptors. Energy taxis receptors perceive changes in energy-related parameters, including signals related to the redox and/or intracellular energy status of the cell. The best-characterized energy taxis receptors are those that sense the redox state of the electron transport chain via non-covalently bound FAD cofactors. Other receptors shown to mediate energy taxis lack any recognizable redox cofactor or conserved energy-sensing motif, and some have been suggested to monitor changes in the proton motive force. The exact energy-sensing mechanism(s) involved are yet to be elucidated for most of these energy sensors. By monitoring changes in energy-related parameters, energy taxis receptors allow cells to couple motility behaviour with metabolism under diverse environmental conditions. Energy taxis receptors thus provide fruitful models to decipher how cells integrate sensory behaviours with metabolic activities.

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2010-08-01
2019-10-17
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References

  1. Alexandre, G., Greer, S. E. & Zhulin, I. B. ( 2000; ). Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 182, 6042–6048.[CrossRef]
    [Google Scholar]
  2. Alexandre, G., Greer-Phillips, S. E. & Zhulin, I. B. ( 2004; ). Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev 28, 113–126.[CrossRef]
    [Google Scholar]
  3. Alvarez-Ortega, C. & Harwood, C. S. ( 2007; ). Identification of a malate chemoreceptor in Pseudomonas aeruginosa by screening for chemotaxis defects in an energy taxis deficient mutant. Appl Environ Microbiol 73, 7793–7795.[CrossRef]
    [Google Scholar]
  4. Ames, P., Studdert, C. A., Reiser, R. H. & Parkinson, J. S. ( 2002; ). Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci U S A 99, 7060–7065.[CrossRef]
    [Google Scholar]
  5. Aravind, L. & Pontig, C. P. ( 1999; ). The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176, 111–116.[CrossRef]
    [Google Scholar]
  6. Bai, F., Branch, R. W., Nicolau, D. V., Jr, Pilizota, T., Steel, B. C., Maini, P. K. & Berry, R. M. ( 2010; ). Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327, 685–689.[CrossRef]
    [Google Scholar]
  7. Baraquet, C., Theraulaz, L., Iobbi-Nivol, C., Mejean, V. & Jourlain-Castelli, C. ( 2009; ). Unexpected chemoreceptors mediate energy taxis towards electron acceptors in Shewanella oneidensis. Mol Microbiol 73, 278–290.[CrossRef]
    [Google Scholar]
  8. Barraud, N., Schleheck, D., Klebensberger, J., Webb, J. S., Hassett, D. J., Rice, S. A. & Kjelleberg, S. ( 2009; ). Nitric oxide signaling in Pseudomonas aeruginosa biofilm mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191, 7333–7342.[CrossRef]
    [Google Scholar]
  9. Berg, H. C. ( 2003; ). The rotary motor of the bacterial flagella. Annu Rev Biochem 72, 19–54.[CrossRef]
    [Google Scholar]
  10. Besschetnova, T. Y., Montefusco, D. J., Asinas, A. E., Shrout, A. L., Antommattei, F. M. & Weis, R. M. ( 2008; ). Receptor density balances signal stimulation and attenuation in membrane-assembled complexes of bacterial chemotaxis signaling proteins. Proc Natl Acad Sci U S A 105, 12289–12294.[CrossRef]
    [Google Scholar]
  11. Bhaya, D. ( 2004; ). Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Mol Microbiol 53, 745–754.[CrossRef]
    [Google Scholar]
  12. Bibikov, S. I., Biran, R., Rudd, K. E. & Parkinson, J. S. ( 1997; ). A signal transducer for aerotaxis in Escherichia coli. J Bacteriol 179, 4075–4079.
    [Google Scholar]
  13. Bibikov, S. I., Barnes, L. A., Gitin, Y. & Parkinson, J. S. ( 2000; ). Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proc Natl Acad Sci U S A 97, 5830–5835.[CrossRef]
    [Google Scholar]
  14. Bibikov, S. I., Miller, A. C., Gosink, K. K. & Parkinson, J. S. ( 2004; ). Methylation-independent aerotaxis mediated by the Escherichia coli Aer protein. J Bacteriol 186, 3730–3737.[CrossRef]
    [Google Scholar]
  15. Bible, A. N., Stephens, B. B., Ortega, D. R., Xie, Z. & Alexandre, G. ( 2008; ). Function of a chemotaxis-like signal transduction pathway in modulating motility, cell clumping and cell length in the alpha-proteobacterium Azospirillum brasilense. J Bacteriol 190, 6365–6375.[CrossRef]
    [Google Scholar]
  16. Bray, D., Levin, M. D. & Morton-Firth, C. J. ( 1998; ). Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88.[CrossRef]
    [Google Scholar]
  17. Briegel, A., Ortega, D. R., Tocheva, E. I., Wuichet, K., Li, Z., Chen, S., Muller, A., Iancu, C., Murphy, G. E. & other authors ( 2009; ). Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci U S A 106, 17181–17186.[CrossRef]
    [Google Scholar]
  18. Croxen, M. A., Sisson, G., Melano, R. & Hoffman, P. S. ( 2006; ). The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for the colonization of the gastric mucosa. J Bacteriol 188, 2656–2665.[CrossRef]
    [Google Scholar]
  19. Edwards, J. C., Johnson, M. S. & Taylor, B. L. ( 2006; ). Differentiation between electron transport sensing and proton motive force sensing by the Aer and Tsr receptors for aerotaxis. Mol Microbiol 62, 823–837.[CrossRef]
    [Google Scholar]
  20. Elliott, K. T., Zhulin, I. B., Stuckey, J. A. & DiRita, V. J. ( 2009; ). Conserved residues in the HAMP domain define a new family of proposed bipartite energy taxis receptors. J Bacteriol 191, 375–387.[CrossRef]
    [Google Scholar]
  21. Ferrandez, A., Hawkins, A. C., Summerfield, D. T. & Harwood, C. S. ( 2002; ). Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotaxis response. J Bacteriol 184, 4374–4383.[CrossRef]
    [Google Scholar]
  22. Fu, R., Wall, J. D. & Voordouw, G. ( 1994; ). DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. J Bacteriol 176, 344–350.
    [Google Scholar]
  23. Gauden, D. E. & Armitage, J. P. ( 1995; ). Electron transport-dependent taxis in Rhodobacter sphaeroides. J Bacteriol 177, 5853–5859.
    [Google Scholar]
  24. Gestwicki, J. E., Lamanna, A. C., Harshey, R. M., McCarter, L. L., Kiessling, L. L. & Adler, J. ( 2000; ). Evolutionary conservation of methyl-accepting chemotaxis protein location in Bacteria and Archaea. J Bacteriol 182, 6499–6502.[CrossRef]
    [Google Scholar]
  25. Goldstein, R. A. & Soyer, O. S. ( 2008; ). Evolution of taxis responses in virtual bacteria: non-adaptive dynamics. PLOS Comput Biol 4, e1000084 [CrossRef]
    [Google Scholar]
  26. Greer-Phillips, S. E., Alexandre, G., Taylor, B. L. & Zhulin, I. B. ( 2003; ). Aer and Tsr guide Escherichia coli in spatial gradients of oxidizable substrates. Microbiology 149, 2661–2667.[CrossRef]
    [Google Scholar]
  27. Greer-Phillips, S. E., Stephens, B. B. & Alexandre, G. ( 2004; ). An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186, 6595–6604.[CrossRef]
    [Google Scholar]
  28. Grishanin, R. N., Gauden, D. E. & Armitage, J. P. ( 1997; ). Photoresponses in Rhodobacter sphaeroides: role of photosynthetic electron transport. J Bacteriol 179, 24–30.
    [Google Scholar]
  29. Hartley-Tassell, L. E., Shewell, L. K., Day, C. J., Wilson, J. C., Sandhu, R., Ketley, J. M. & Korolik, V. ( 2010; ). Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni. Mol Microbiol 75, 710–730.
    [Google Scholar]
  30. Hazelbauer, G. L., Falke, J. J. & Parkinson, J. S. ( 2008; ). Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33, 9–19.[CrossRef]
    [Google Scholar]
  31. Hendrixson, D. R., Aklerley, B. J. & Di Rita, V. ( 2001; ). Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40, 214–224.[CrossRef]
    [Google Scholar]
  32. Hickman, J. W., Tifrea, T. F. & Harwood, C. S. ( 2005; ). A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102, 14422–14427.[CrossRef]
    [Google Scholar]
  33. Hoff, W. D., van der Horst, M. A., Nudel, C. B. & Hellingwerf, K. J. ( 2009; ). Prokaryotic phototaxis. Methods Mol Biol 571, 25–49.
    [Google Scholar]
  34. Hong, C. S., Shitashiro, M., Kuroda, A., Ikeda, T., Takiguchi, N., Ohtake, H. & Kato, J. ( 2004; ). Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa. FEMS Microbiol Lett 231, 247–252.[CrossRef]
    [Google Scholar]
  35. Hou, S., Larsen, R. W., Boudko, D., Riley, C. W., Karatan, E., Zimmer, M., Ordal, G. W. & Alam, M. ( 2000; ). Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544.[CrossRef]
    [Google Scholar]
  36. Jiang, Z. Y. & Bauer, C. E. ( 2001; ). Component of the Rhodospirillum centenum photosensory apparatus with structural and functional similarity to methyl-accepting chemotaxis protein chemoreceptors. J Bacteriol 183, 171–177.[CrossRef]
    [Google Scholar]
  37. Jiang, Z.-Y., Gest, H. & Bauer, C. E. ( 1997; ). Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J Bacteriol 179, 5720–5727.
    [Google Scholar]
  38. Kentner, D., Thiem, S., Hildenbeutel, M. & Sourjik, V. ( 2006; ). Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61, 407–417.[CrossRef]
    [Google Scholar]
  39. Kirby, J. R. ( 2009; ). Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annu Rev Microbiol 63, 45–59.[CrossRef]
    [Google Scholar]
  40. Lai, R. Z., Manson, J. M., Bormans, A. F., Draheim, R. R., Nguyen, N. T. & Manson, M. D. ( 2005; ). Cooperative signaling among bacterial chemoreceptors. Biochemistry 44, 14298–14307.[CrossRef]
    [Google Scholar]
  41. Levit, M. N. & Stock, J. B. ( 1999; ). pH sensing in bacterial chemotaxis. Novartis Found Symp 221, 38–50.
    [Google Scholar]
  42. Li, J., Go, A. C., Ward, M. J. & Ottemann, K. M. ( 2010; ). The chemical-in-plug bacterial chemotaxis assay is prone to false positive responses. BMC Res Notes 3, 77–81.[CrossRef]
    [Google Scholar]
  43. Mascher, T., Helmann, J. D. & Unden, G. ( 2006; ). Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70, 910–938.[CrossRef]
    [Google Scholar]
  44. Miller, J. B. & Koshland, D. E., Jr ( 1980; ). Protonmotive force and bacterial sensing. J Bacteriol 141, 26–32.
    [Google Scholar]
  45. Miller, L. D., Russell, M. H. & Alexandre, G. ( 2009; ). Diversity in bacterial chemotactic responses and niche adaptation. Adv Appl Microbiol 66, 53–75.
    [Google Scholar]
  46. Morgan, R., Kohn, S., Hwang, S. H., Hassett, D. J. & Sauer, K. ( 2006; ). BldA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 188, 7335–7343.[CrossRef]
    [Google Scholar]
  47. Niwano, M. & Taylor, B. L. ( 1982; ). Novel sensory adaptation mechanism in bacterial chemotaxis to oxygen and phosphotransferase substrates. Proc Natl Acad Sci U S A 79, 11–15.[CrossRef]
    [Google Scholar]
  48. Rebbapragada, A., Johnson, M. S., Harding, G. P., Zuccarelli, A. J., Fletcher, H. M., Zhulin, I. B. & Taylor, B. L. ( 1997; ). 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 U S A 94, 10541–10546.[CrossRef]
    [Google Scholar]
  49. Repik, A., Rebbapragada, A., Johnson, M. S., Haznedar, J. O., Zhulin, I. B. & Taylor, B. L. ( 2000; ). PAS domain residues involved in signal transduction by the Aer redox sensor of Escherichia coli. Mol Microbiol 36, 806–816.[CrossRef]
    [Google Scholar]
  50. Rowsell, E. H., Smith, J. M., Wolfe, A. & Taylor, B. L. ( 1995; ). CheA, CheW, and CheY are required for chemotaxis to oxygen and sugars of the phosphotransferase system in Escherichia coli. J Bacteriol 177, 6011–6014.
    [Google Scholar]
  51. Salman, H. & Libchaber, A. ( 2007; ). A concentration-dependent switch in the bacterial response to temperature. Nat Cell Biol 9, 1098–1100.[CrossRef]
    [Google Scholar]
  52. Sarand, I., Osterberg, S., Holmqvist, S., Holmfeldt, P., Skarfstad, E., Parales, R. E. & Shingler, V. ( 2008; ). Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of the three polar localized Aer-like proteins of Pseudomonas putida. Environ Microbiol 10, 1320–1334.[CrossRef]
    [Google Scholar]
  53. Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A., Davies, D. G. & Gilbert, P. ( 2004; ). Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186, 7312–7326.[CrossRef]
    [Google Scholar]
  54. Schreiber, S., Konradt, M., Groll, C., Scheid, P., Hanauer, G., Werling, H.-O., Josenhans, C. & Suerbaum, S. ( 2004; ). The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci U S A 101, 5024–5029.[CrossRef]
    [Google Scholar]
  55. Schweinitzer, T. & Josenhans, C. ( 2010; ). Bacterial energy taxis: a global strategy? Arch Microbiol [Epub ahead of print]
    [Google Scholar]
  56. Schweinitzer, T., Mizote, T., Ishikawa, N., Dudnik, A., Inatsu, S., Schreiber, S., Suerbaum, S., Aizawa, S.-I. & Josenhans, C. ( 2008; ). Functional characterization and mutagenesis of the proposed behavioral sensor TlpD of Helicobacter pylori. J Bacteriol 190, 3244–3255.[CrossRef]
    [Google Scholar]
  57. Shioi, J., Tribhuwan, R. C., Berg, S. T. & Taylor, B. L. ( 1988; ). Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium. J Bacteriol 170, 5507–5511.
    [Google Scholar]
  58. Slonczewski, J. L., Macnab, R. M., Alger, J. R. & Castle, A. ( 1982; ). Effects of pH and repellent tactic stimuli on protein methylation levels in Escherichia coli. J Bacteriol 152, 384–399.
    [Google Scholar]
  59. Sourjik, V. & Berg, H. C. ( 2004; ). Functional interactions between receptors in bacterial chemotaxis. Nature 428, 437–441.[CrossRef]
    [Google Scholar]
  60. Stephens, B. B., Loar, S. N. & Alexandre, G. ( 2006; ). Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense. J Bacteriol 188, 4759–4768.[CrossRef]
    [Google Scholar]
  61. Stingl, K., Uhlemann, E. M., Schmid, R., Altendorf, K. & Bakker, E. P. ( 2002; ). Energetics of Helicobacter pylori and its implications for the mechanism of urease-dependent acid tolerance at pH 1. J Bacteriol 184, 3053–3060.[CrossRef]
    [Google Scholar]
  62. Stock, A. M., Robinson, V. L. & Goudreau, P. N. ( 2000; ). Two-component signal transduction. Annu Rev Biochem 69, 183–215.[CrossRef]
    [Google Scholar]
  63. Studdert, C. A. & Parkinson, J. S. ( 2004; ). Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci U S A 101, 2117–2122.[CrossRef]
    [Google Scholar]
  64. Szurmant, H. & Ordal, G. W. ( 2004; ). Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68, 301–319.[CrossRef]
    [Google Scholar]
  65. Taylor, B. L. ( 2007; ). Aer on the inside looking out: paradigm for a PAS-HAMP role in sensing oxygen, redox and energy. Mol Microbiol 65, 1415–1424.[CrossRef]
    [Google Scholar]
  66. Taylor, B. L., Zhulin, I. B. & Johnson, M. S. ( 1999; ). Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53, 103–128.[CrossRef]
    [Google Scholar]
  67. Ulrich, L. E. & Zhulin, I. B. ( 2010; ). MIST2: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res 38, D401–D407.[CrossRef]
    [Google Scholar]
  68. Umemura, T., Matsumoto, Y., Ohnishi, K., Homma, M. & Kawagishi, I. ( 2002; ). Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J Biol Chem 277, 1593–1598.[CrossRef]
    [Google Scholar]
  69. Vegge, C. S., Bonsdsted, L., Li, Y.-P., Bang, D. D. & Ingmer, H. ( 2009; ). Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth. Appl Environ Microbiol 75, 5308–5314.[CrossRef]
    [Google Scholar]
  70. Wadhams, G. H. & Armitage, J. P. ( 2004; ). Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5, 1024–1037.[CrossRef]
    [Google Scholar]
  71. Watts, K. J., Johnson, M. S. & Taylor, B. L. ( 2004; ). Interactions between the PAS and HAMP domain of the Escherichia coli aerotaxis receptor Aer. J Bacteriol 186, 7440–7449.[CrossRef]
    [Google Scholar]
  72. Wuichet, K., Alexander, R. P. & Zhulin, I. B. ( 2007; ). Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol 422, 1–31.
    [Google Scholar]
  73. Xie, Z., Ulrich, L. E., Zhulin, I. B. & Alexandre, G. ( 2010; ). PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis. Proc Natl Acad Sci U S A 107, 2235–2240.[CrossRef]
    [Google Scholar]
  74. Yao, J. & Allen, C. ( 2007; ). The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interaction with its tomato host. J Bacteriol 189, 6415–6424.[CrossRef]
    [Google Scholar]
  75. Yoshihara, S. & Ikeuchi, M. ( 2004; ). Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol Sci 3, 512–518.[CrossRef]
    [Google Scholar]
  76. Yost, C. K., Rochepeau, P. & Hynes, M. F. ( 1998; ). Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144, 1945–1956.[CrossRef]
    [Google Scholar]
  77. Zhulin, I. B. ( 2001; ). The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv Microb Physiol 45, 157–198.
    [Google Scholar]
  78. Zhulin, I. B. & Armitage, J. P. ( 1993; ). Motility, chemokinesis, and methylation-independent chemotaxis in Azospirillum brasilense. J Bacteriol 175, 952–958.
    [Google Scholar]
  79. Zhulin, I. B., Bespalov, V. A., Johnson, M. S. & Taylor, B. L. ( 1996; ). Oxygen taxis and proton motive force in Azospirillum brasilense. J Bacteriol 178, 5199–5204.
    [Google Scholar]
  80. Zhulin, I. B., Rowsell, E. H., Johnson, M. S. & Taylor, B. L. ( 1997; ). Glycerol elicits energy taxis of Escherichia coli and Salmonella typhimurium. J Bacteriol 179, 3196–3201.
    [Google Scholar]
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