Bacterial energy taxis: a global strategy?

A functional energy metabolism is one of the most important requirements for survival of all kinds of organisms including bacteria. Therefore, many bacteria actively seek conditions of optimal metabolic activity, a behaviour which can be termed “energy taxis”. Motility, combined with the sensory perception of the internal energetic conditions, is prerequisite for tactic responses to different energy levels and metabolic yields. Diverse mechanisms of energy sensing and tactic response have evolved among various bacteria. Many of the known energy taxis sensors group among the methyl-accepting chemotaxis protein (MCP)-like sensors. This review summarizes recent advances in the field of energy taxis and explores the current concept that energy taxis is an important part of the bacterial behavioural repertoire in order to navigate towards more favourable metabolic niches and to survive in a specific habitat.

[1]  C. Lancaster,et al.  Succinate:quinone oxidoreductases from epsilon-proteobacteria. , 2002, Biochimica et biophysica acta.

[2]  C. Harwood,et al.  An aerotaxis transducer gene from Pseudomonas putida. , 2000, FEMS microbiology letters.

[3]  C. Josenhans,et al.  Functional Characterization and Mutagenesis of the Proposed Behavioral Sensor TlpD of Helicobacter pylori , 2008, Journal of bacteriology.

[4]  J. Shapleigh,et al.  Taxis Response of Various Denitrifying Bacteria to Nitrate and Nitrite , 2002, Applied and Environmental Microbiology.

[5]  K. Ottemann,et al.  Colonization and Inflammation Deficiencies in Mongolian Gerbils Infected by Helicobacter pylori Chemotaxis Mutants , 2005, Infection and Immunity.

[6]  B. L. Taylor,et al.  Differentiation between electron transport sensing and proton motive force sensing by the Aer and Tsr receptors for aerotaxis , 2006, Molecular microbiology.

[7]  G. Nyakatura,et al.  The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Dieter Jahn,et al.  Fermentative Metabolism of Bacillus subtilis: Physiology and Regulation of Gene Expression , 2000, Journal of bacteriology.

[9]  J. Kirby,et al.  Predataxis behavior in Myxococcus xanthus , 2008, Proceedings of the National Academy of Sciences.

[10]  C. Josenhans,et al.  Rapid Loss of Motility of Helicobacter pylori in the Gastric Lumen In Vivo , 2005, Infection and Immunity.

[11]  D. Haas,et al.  Positive FNR-like control of anaerobic arginine degradation and nitrate respiration in Pseudomonas aeruginosa , 1991, Journal of bacteriology.

[12]  M. Alam,et al.  Myoglobin-like aerotaxis transducers in Archaea and Bacteria , 2000, Nature.

[13]  K. Amako,et al.  Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract , 1992, Infection and immunity.

[14]  J. S. Parkinson,et al.  Loss- and Gain-of-Function Mutations in the F1-HAMP Region of the Escherichia coli Aerotaxis Transducer Aer , 2006, Journal of bacteriology.

[15]  Peer Bork,et al.  SMART 6: recent updates and new developments , 2008, Nucleic Acids Res..

[16]  Igor B. Zhulin,et al.  The MiST2 database: a comprehensive genomics resource on microbial signal transduction , 2009, Nucleic Acids Res..

[17]  I. Zhulin,et al.  PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light , 1999, Microbiology and Molecular Biology Reviews.

[18]  K. Hellingwerf,et al.  Conformational heterogeneity and propagation of structural changes in the LOV2/Jalpha domain from Avena sativa phototropin 1 as recorded by temperature-dependent FTIR spectroscopy. , 2009, Biophysical journal.

[19]  K. Stingl,et al.  Energetics of Helicobacter pylori and Its Implications for the Mechanism of Urease-Dependent Acid Tolerance at pH 1 , 2002, Journal of bacteriology.

[20]  I. Zhulin,et al.  Conserved Residues in the HAMP Domain Define a New Family of Proposed Bipartite Energy Taxis Receptors , 2008, Journal of bacteriology.

[21]  G. Unden,et al.  Changes in the proton potential and the cellular energetics of Escherichia coli during growth by aerobic and anaerobic respiration or by fermentation. , 1998, European journal of biochemistry.

[22]  J. Spudich,et al.  Properties of a second sensory receptor protein in Halobacterium halobium phototaxis , 1986, Proteins.

[23]  R. Haas,et al.  Identification and Characterization of Helicobacter pylori Genes Essential for Gastric Colonization , 2003, The Journal of experimental medicine.

[24]  George M. Hilliard,et al.  Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. , 2002, Developmental cell.

[25]  R. Melano,et al.  The Helicobacter pylori Chemotaxis Receptor TlpB (HP0103) Is Required for pH Taxis and for Colonization of the Gastric Mucosa , 2006, Journal of bacteriology.

[26]  J. Stülke,et al.  Trigger enzymes: bifunctional proteins active in metabolism and in controlling gene expression , 2007, Molecular microbiology.

[27]  G. Alexandre,et al.  Diversity in bacterial chemotactic responses and niche adaptation. , 2009, Advances in applied microbiology.

[28]  S. Butler,et al.  Selection for in vivo regulators of bacterial virulence , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  I. Zhulin,et al.  Role of methylation in aerotaxis in Bacillus subtilis , 1995, Journal of bacteriology.

[30]  D. Koshland,et al.  Electron acceptor taxis and blue light effect on bacterial chemotaxis , 1979, Journal of bacteriology.

[31]  V. DiRita,et al.  Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility , 2001, Molecular microbiology.

[32]  I. Zhulin,et al.  Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough , 1997, Journal of bacteriology.

[33]  Igor B Zhulin,et al.  Aer and Tsr guide Escherichia coli in spatial gradients of oxidizable substrates. , 2003, Microbiology.

[34]  G. Alexandre,et al.  An Energy Taxis Transducer Promotes Root Colonization by Azospirillum brasilense , 2004, Journal of bacteriology.

[35]  J. Adler,et al.  Chemoreceptors in bacteria. , 1969, Science.

[36]  S. Khan,et al.  Chemotactic signal integration in bacteria. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  K. Ottemann,et al.  Helicobacter pylori Chemotaxis Modulates Inflammation and Bacterium-Gastric Epithelium Interactions in Infected Mice , 2007, Infection and Immunity.

[38]  G. Ordal,et al.  Chemotaxis towards sugars by Bacillus subtilis. , 1979, Journal of general microbiology.

[39]  S. M. Horne,et al.  An Escherichia coli aer mutant exhibits a reduced ability to colonize the streptomycin-treated mouse large intestine , 2009, Antonie van Leeuwenhoek.

[40]  H. Ohtake,et al.  Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa. , 2004, FEMS microbiology letters.

[41]  A. Losi,et al.  Bacterial bilin- and flavin-binding photoreceptors , 2008, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[42]  Hendrik Szurmant,et al.  Diversity in Chemotaxis Mechanisms among the Bacteria and Archaea , 2004, Microbiology and Molecular Biology Reviews.

[43]  Ralph Schlapbach,et al.  Genome‐wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori , 2004, Molecular microbiology.

[44]  B. L. Taylor Aer on the inside looking out: paradigm for a PAS–HAMP role in sensing oxygen, redox and energy , 2007, Molecular microbiology.

[45]  Judith P. Armitage,et al.  Light-induced behavioral responses (`phototaxis') in prokaryotes , 2004, Photosynthesis Research.

[46]  R. Ye,et al.  Global Gene Expression Profiles of Bacillus subtilis Grown under Anaerobic Conditions , 2000, Journal of bacteriology.

[47]  M. Nakano,et al.  Anaerobic growth of a "strict aerobe" (Bacillus subtilis). , 1998, Annual review of microbiology.

[48]  I. Zhulin,et al.  Oxygen taxis and proton motive force in Azospirillum brasilense , 1996, Journal of bacteriology.

[49]  C. Josenhans,et al.  Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes , 1996, Infection and immunity.

[50]  J. Kirby,et al.  Chemotaxis-like regulatory systems: unique roles in diverse bacteria. , 2009, Annual review of microbiology.

[51]  J. Kirby,et al.  Chemosensory regulation of developmental gene expression in Myxococcus xanthus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  D. Bhaya,et al.  Multiple Light Inputs Control Phototaxis in Synechocystis sp. Strain PCC6803 , 2003, Journal of bacteriology.

[53]  J. Sancho,et al.  Flavodoxin:Quinone Reductase (FqrB): a Redox Partner of Pyruvate:Ferredoxin Oxidoreductase That Reversibly Couples Pyruvate Oxidation to NADPH Production in Helicobacter pylori and Campylobacter jejuni , 2007, Journal of bacteriology.

[54]  Johan Auwerx,et al.  PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure , 2009, Current opinion in lipidology.

[55]  Jian Yao,et al.  Chemotaxis Is Required for Virulence and Competitive Fitness of the Bacterial Wilt Pathogen Ralstonia solanacearum , 2006, Journal of bacteriology.

[56]  B. Wren,et al.  Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. , 2002, Trends in microbiology.

[57]  C. Josenhans,et al.  The spatial orientation of Helicobacter pylori in the gastric mucus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[58]  W. Zhang,et al.  Signal transduction in the archaeon Halobacterium salinarium is processed through three subfamilies of 13 soluble and membrane-bound transducer proteins. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[59]  R. Weingarten,et al.  Role of Campylobacter jejuni Respiratory Oxidases and Reductases in Host Colonization , 2008, Applied and Environmental Microbiology.

[60]  A. Bren,et al.  How Signals Are Heard during Bacterial Chemotaxis: Protein-Protein Interactions in Sensory Signal Propagation , 2000, Journal of bacteriology.

[61]  J. Armitage,et al.  Electron transport-dependent taxis in Rhodobacter sphaeroides , 1995, Journal of bacteriology.

[62]  J. W. Campbell,et al.  FlhD/FlhC Is a Regulator of Anaerobic Respiration and the Entner-Doudoroff Pathway through Induction of the Methyl-Accepting Chemotaxis Protein Aer , 2003, Journal of bacteriology.

[63]  G. Wadhams,et al.  Making sense of it all: bacterial chemotaxis , 2004, Nature Reviews Molecular Cell Biology.

[64]  M. Homma,et al.  Sensing of Cytoplasmic pH by Bacterial Chemoreceptors Involves the Linker Region That Connects the Membrane-spanning and the Signal-modulating Helices* , 2002, The Journal of Biological Chemistry.

[65]  J. Wall,et al.  DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment , 1994, Journal of bacteriology.

[66]  J. S. Parkinson,et al.  Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Stock,et al.  Bacterial chemotaxis , 2003, Current Biology.

[68]  C. Boucher,et al.  Lessons learned from the genome analysis of ralstonia solanacearum. , 2004, Annual review of phytopathology.

[69]  Noboru Takiguchi,et al.  Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. , 2008, Journal of bioscience and bioengineering.

[70]  J. Ram,et al.  Bacterial chemotaxis differences in Escherichia coli isolated from different hosts. , 2008, Canadian journal of microbiology.

[71]  I. Zhulin,et al.  Aerotaxis and other energy-sensing behavior in bacteria. , 1999, Annual review of microbiology.

[72]  Ashlee M Earl,et al.  Ecology and genomics of Bacillus subtilis. , 2008, Trends in microbiology.

[73]  I. Zhulin,et al.  Ecological role of energy taxis in microorganisms. , 2004, FEMS microbiology reviews.

[74]  I. Zhulin,et al.  Behavioral responses of Escherichia coli to changes in redox potential. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  J. S. Parkinson,et al.  Bacterial chemoreceptors: high-performance signaling in networked arrays. , 2008, Trends in biochemical sciences.

[76]  J. S. Parkinson,et al.  Methylation-Independent Aerotaxis Mediated by the Escherichia coli Aer Protein , 2004, Journal of bacteriology.

[77]  M. A. van der Horst,et al.  Prokaryotic phototaxis. , 2009, Methods in molecular biology.

[78]  A. Rebbapragada,et al.  The FAD-PAS domain as a sensor for behavioral responses in Escherichia coli. , 2001, Antioxidants & redox signaling.

[79]  M. Alam,et al.  An Archaeal Aerotaxis Transducer Combines Subunit I Core Structures of Eukaryotic Cytochrome c Oxidase and Eubacterial Methyl-Accepting Chemotaxis Proteins , 1998, Journal of bacteriology.

[80]  V. DiRita,et al.  Characterization of CetA and CetB, a bipartite energy taxis system in Campylobacter jejuni , 2008, Molecular microbiology.

[81]  C. Bauer,et al.  A che‐like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum , 2005, Molecular microbiology.

[82]  J. Ingraham,et al.  Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans , 1983, Applied and environmental microbiology.

[83]  Jian Yao,et al.  The Plant Pathogen Ralstonia solanacearum Needs Aerotaxis for Normal Biofilm Formation and Interactions with Its Tomato Host , 2007, Journal of bacteriology.

[84]  Hideaki Yoshimura,et al.  Protein Conformation Changes of HemAT-Bs upon Ligand Binding Probed by Ultraviolet Resonance Raman Spectroscopy* , 2008, Journal of Biological Chemistry.

[85]  H. Ingmer,et al.  Energy Taxis Drives Campylobacter jejuni toward the Most Favorable Conditions for Growth , 2009, Applied and Environmental Microbiology.

[86]  J. Spudich,et al.  Primary structure of an archaebacterial transducer, a methyl-accepting protein associated with sensory rhodopsin I. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[87]  H. Ohtake,et al.  The aerotaxis transducer gene aer, but not aer-2, is transcriptionally regulated by the anaerobic regulator ANR in Pseudomonas aeruginosa. , 2004, Journal of bioscience and bioengineering.

[88]  I. Zhulin,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. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[89]  J. Auwerx,et al.  Transcriptional coregulators in the control of energy homeostasis. , 2007, Trends in cell biology.

[90]  K. Weber,et al.  Behavioral response of dissimilatory perchlorate-reducing bacteria to different electron acceptors , 2009, Applied Microbiology and Biotechnology.

[91]  C. Jourlin-Castelli,et al.  Unexpected chemoreceptors mediate energy taxis towards electron acceptors in Shewanella oneidensis , 2009, Molecular microbiology.

[92]  D. Burr,et al.  CheY‐mediated modulation of Campylobacter jejuni virulence , 1997, Molecular microbiology.

[93]  S. Hall,et al.  Growth of Campylobacter jejuni Supported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen , 2002, Journal of bacteriology.

[94]  D. Beier,et al.  Molecular Characterization of Two-Component Systems of Helicobacter pylori , 2000, Journal of bacteriology.

[95]  Igor B. Zhulin,et al.  Energy Taxis Is the Dominant Behavior in Azospirillum brasilense , 2000, Journal of bacteriology.

[96]  Mark S. Johnson,et al.  Structure-Function Relationships in the HAMP and Proximal Signaling Domains of the Aerotaxis Receptor Aer , 2008, Journal of bacteriology.

[97]  D. Hilbert,et al.  Sporulation of Bacillus subtilis. , 2004, Current opinion in microbiology.

[98]  C. Taylor Mitochondria and cellular oxygen sensing in the HIF pathway. , 2008, The Biochemical journal.

[99]  Luke E. Ulrich,et al.  PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis , 2010, Proceedings of the National Academy of Sciences of the United States of America.

[100]  C. Bauer,et al.  Involvement of a Che‐like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum , 2005, Molecular microbiology.

[101]  M Lebert,et al.  Methyl‐accepting taxis proteins in Halobacterium halobium. , 1989, The EMBO journal.

[102]  A. Piérard,et al.  Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway , 1984, Journal of bacteriology.

[103]  Y. Imae,et al.  Thermosensing properties of Escherichia coli tsr mutants defective in serine chemoreception , 1988, Journal of bacteriology.

[104]  C. Häse,et al.  Characterization of Vibrio cholerae aerotaxis. , 2007, FEMS microbiology letters.

[105]  Mark S. Johnson,et al.  Topology and Boundaries of the Aerotaxis Receptor Aer in the Membrane of Escherichia coli , 2006, Journal of bacteriology.