Comparative Genomic Evidence for a Close Relationship between the Dimorphic Prosthecate Bacteria Hyphomonas neptunium and Caulobacter crescentus

ABSTRACT The dimorphic prosthecate bacteria (DPB) are α-proteobacteria that reproduce in an asymmetric manner rather than by binary fission and are of interest as simple models of development. Prior to this work, the only member of this group for which genome sequence was available was the model freshwater organism Caulobacter crescentus. Here we describe the genome sequence of Hyphomonas neptunium, a marine member of the DPB that differs from C. crescentus in that H. neptunium uses its stalk as a reproductive structure. Genome analysis indicates that this organism shares more genes with C. crescentus than it does with Silicibacter pomeroyi (a closer relative according to 16S rRNA phylogeny), that it relies upon a heterotrophic strategy utilizing a wide range of substrates, that its cell cycle is likely to be regulated in a similar manner to that of C. crescentus, and that the outer membrane complements of H. neptunium and C. crescentus are remarkably similar. H. neptunium swarmer cells are highly motile via a single polar flagellum. With the exception of cheY and cheR, genes required for chemotaxis were absent in the H. neptunium genome. Consistent with this observation, H. neptunium swarmer cells did not respond to any chemotactic stimuli that were tested, which suggests that H. neptunium motility is a random dispersal mechanism for swarmer cells rather than a stimulus-controlled navigation system for locating specific environments. In addition to providing insights into bacterial development, the H. neptunium genome will provide an important resource for the study of other interesting biological processes including chromosome segregation, polar growth, and cell aging.

[1]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[2]  Jeffrey M. Skerker,et al.  A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus , 2006, Molecular microbiology.

[3]  J. Poindexter Dimorphic Prosthecate Bacteria: The Genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron , 2006 .

[4]  A. Nordheim,et al.  ExbBD-Dependent Transport of Maltodextrins through the Novel MalA Protein across the Outer Membrane of Caulobacter crescentus , 2005, Journal of bacteriology.

[5]  Michael T Laub,et al.  Two-Component Signal Transduction Pathways Regulating Growth and Cell Cycle Progression in a Bacterium: A System-Level Analysis , 2005, PLoS biology.

[6]  Kyung-Bum Lee,et al.  The hierarchical system of the 'Alphaproteobacteria': description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. , 2005, International journal of systematic and evolutionary microbiology.

[7]  Ian T. Paulsen,et al.  Comparative Analyses of Fundamental Differences in Membrane Transport Capabilities in Prokaryotes and Eukaryotes , 2005, PLoS Comput. Biol..

[8]  Damon A. Clark,et al.  The bacterial chemotactic response reflects a compromise between transient and steady-state behavior. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Gerdes,et al.  Prokaryotic toxin–antitoxin stress response loci , 2005, Nature Reviews Microbiology.

[10]  François Taddei,et al.  Aging and Death in an Organism That Reproduces by Morphologically Symmetric Division , 2005, PLoS Biology.

[11]  Owen White,et al.  Genome Properties: a system for the investigation of prokaryotic genetic content for microbiology, genome annotation and comparative genomics , 2005, Bioinform..

[12]  Jay X. Tang,et al.  The Elastic Properties of the Caulobacter crescentus Adhesive Holdfast Are Dependent on Oligomers of N-Acetylglucosamine , 2005, Journal of bacteriology.

[13]  E. Leifson Hyphomicrobium neptunium sp. n. , 2005, Antonie van Leeuwenhoek.

[14]  Ian T. Paulsen,et al.  Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment , 2004, Nature.

[15]  A. Bairoch,et al.  The Swiss-Prot protein knowledgebase and ExPASy: providing the plant community with high quality proteomic data and tools. , 2004, Plant physiology and biochemistry : PPB.

[16]  J. Gober,et al.  Regulation of FlbD activity by flagellum assembly is accomplished through direct interaction with the trans‐acting factor, FliX , 2004, Molecular microbiology.

[17]  Paul G. Falkowski,et al.  The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway , 2004 .

[18]  Michael T. Laub,et al.  Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus , 2004, Nature Reviews Microbiology.

[19]  Y. Brun,et al.  Development of Surface Adhesion in Caulobacter crescentus , 2004, Journal of bacteriology.

[20]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[21]  H. Engelberg-Kulka,et al.  Bacterial programmed cell death systems as targets for antibiotics. , 2004, Trends in microbiology.

[22]  Ian T. Paulsen,et al.  TransportDB: a relational database of cellular membrane transport systems , 2004, Nucleic Acids Res..

[23]  H. Berg The rotary motor of bacterial flagella. , 2003, Annual review of biochemistry.

[24]  C. Jacobs-Wagner,et al.  Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus. , 2003, Annual review of microbiology.

[25]  Finbarr Hayes,et al.  Toxins-Antitoxins: Plasmid Maintenance, Programmed Cell Death, and Cell Cycle Arrest , 2003, Science.

[26]  Y. Brun,et al.  The HfaB and HfaD adhesion proteins of Caulobacter crescentus are localized in the stalk , 2003, Molecular microbiology.

[27]  K. Borzym,et al.  Complete genome sequence of the marine planctomycete Pirellula sp. strain 1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Martin Ackermann,et al.  Senescence in a Bacterium with Asymmetric Division , 2003, Science.

[29]  T. Nyström Conditional senescence in bacteria: death of the immortals , 2003, Molecular microbiology.

[30]  D. Larson,et al.  Identification of Genes Required for Synthesis of the Adhesive Holdfast in Caulobacter crescentus , 2003, Journal of bacteriology.

[31]  Alex Bateman,et al.  QuickTree: building huge Neighbour-Joining trees of protein sequences , 2002, Bioinform..

[32]  Ingeborg Holt,et al.  The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  D. Kelly,et al.  The prokaryotes: an evolving electronic resource for the microbiological community - , 2002 .

[34]  P. Garrigues Biomarkers in Marine Organisms: A Practical Approach , 2001 .

[35]  S. Salzberg,et al.  Complete Genome Sequence of a Virulent Isolate of Streptococcus pneumoniae , 2001, Science.

[36]  Ian T. Paulsen,et al.  Complete genome sequence of Caulobacter crescentus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Sicheritz-Pontén,et al.  A phylogenomic approach to microbial evolution. , 2001, Nucleic acids research.

[38]  P. Garrigues,et al.  BIOCHEMICAL MARKERS IN MUSSEL, MYTILUS SP., AND POLLUTION MONITORING IN EUROPEAN COASTS : DATA ANALYSIS , 2001 .

[39]  H. McAdams,et al.  Global analysis of the genetic network controlling a bacterial cell cycle. , 2000, Science.

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

[41]  K. Lewis,et al.  Programmed Death in Bacteria , 2000, Microbiology and Molecular Biology Reviews.

[42]  S. Langille,et al.  Polysaccharide-specific probes inhibit adhesion of Hyphomonas rosenbergii strain VP-6 to hydrophilic surfaces , 2000, Journal of Industrial Microbiology and Biotechnology.

[43]  M. Saier A Functional-Phylogenetic Classification System for Transmembrane Solute Transporters , 2000, Microbiology and Molecular Biology Reviews.

[44]  A. Matin,et al.  The G‐protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida , 2000, Molecular microbiology.

[45]  R. Weiner,et al.  Hyphomonas adhaerens sp. nov., Hyphomonas johnsonii sp. nov. and Hyphomonas rosenbergii sp. nov., marine budding and prosthecate bacteria. , 2000, International journal of systematic and evolutionary microbiology.

[46]  R. Ramphal,et al.  fleN, a Gene That Regulates Flagellar Number in Pseudomonas aeruginosa , 2000, Journal of bacteriology.

[47]  A. Newton,et al.  Signal Transduction and Cell Cycle Checkpoints in Developmental Regulation of Caulobacter , 2000 .

[48]  S. Salzberg,et al.  Improved microbial gene identification with GLIMMER. , 1999, Nucleic acids research.

[49]  M. Moran,et al.  Transformation of Sulfur Compounds by an Abundant Lineage of Marine Bacteria in the α-Subclass of the ClassProteobacteria , 1999, Applied and Environmental Microbiology.

[50]  Stefan Kurtz,et al.  REPuter: fast computation of maximal repeats in complete genomes , 1999, Bioinform..

[51]  Lucy Shapiro,et al.  The CtrA Response Regulator Mediates Temporal Control of Gene Expression during the Caulobacter Cell Cycle , 1999, Journal of bacteriology.

[52]  D. Eisenberg,et al.  Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  S. Langille,et al.  Spatial and Temporal Deposition ofHyphomonas Strain VP-6 Capsules Involved in Biofilm Formation , 1998, Applied and Environmental Microbiology.

[55]  R. Weiner,et al.  Spatial and Temporal Deposition of Adhesive Extracellular Polysaccharide Capsule and Fimbriae byHyphomonas Strain MHS-3 , 1998, Applied and Environmental Microbiology.

[56]  R. Huber,et al.  The complete genome of the hyperthermophilic bacterium Aquifex aeolicus , 1998, Nature.

[57]  A. Newton,et al.  Regulation of the Caulobacter flagellar gene hierarchy; not just for motility , 1997, Molecular microbiology.

[58]  M. Kessel,et al.  Fine-structure evidence for cell membrane partitioning of the nucleoid and cytoplasm during bud formation in Hyphomonas species , 1997, Journal of bacteriology.

[59]  M. Otte,et al.  Organism-induced accumulation of iron, zinc and arsenic in wetland soils. , 1997, Environmental pollution.

[60]  S. Karlin,et al.  Frequent oligonucleotides and peptides of the Haemophilus influenzae genome. , 1996, Nucleic acids research.

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

[62]  Lucy Shapiro,et al.  Cell Cycle Control by an Essential Bacterial Two-Component Signal Transduction Protein , 1996, Cell.

[63]  R. Macnab,et al.  Flagella and motility , 1996 .

[64]  A. Benson,et al.  Global regulation of a sigma 54-dependent flagellar gene family in Caulobacter crescentus by the transcriptional activator FlbD , 1995, Journal of bacteriology.

[65]  R. Weiner,et al.  Evidence for the Adhesive Function of the Exopolysaccharide of Hyphomonas Strain MHS-3 in Its Attachment to Surfaces , 1995, Applied and environmental microbiology.

[66]  P. Matsumura,et al.  Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium , 1995 .

[67]  J. Hoch,et al.  Two-component signal transduction , 1995 .

[68]  D. Mullin,et al.  FlbD has a DNA-binding activity near its carboxy terminus that recognizes ftr sequences involved in positive and negative regulation of flagellar gene transcription in Caulobacter crescentus , 1994, Journal of bacteriology.

[69]  A. Ninfa,et al.  The Caulobacter crescentus FlbD protein acts at ftr sequence elements both to activate and to repress transcription of cell cycle-regulated flagellar genes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[70]  J. Wingrove,et al.  Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter. , 1993, Genes & development.

[71]  L. Shapiro,et al.  A temporally controlled sigma-factor is required for polar morphogenesis and normal cell division in Caulobacter. , 1992, Genes & development.

[72]  R. Haas,et al.  Cloning and genetic characterization of a Hellcobacter pylori flagellin gene , 1992, Molecular microbiology.

[73]  Amir Dembo,et al.  Poisson Approximations for $r$-Scan Processes , 1992 .

[74]  S. Lory,et al.  The filA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for flagellin synthesis , 1992, Molecular microbiology.

[75]  H. Kurtz,et al.  Analysis of a Caulobacter crescentus gene cluster involved in attachment of the holdfast to the cell , 1992, Journal of bacteriology.

[76]  A. Newton,et al.  FlbD of Caulobacter crescentus is a homologue of the NtrC (NRI) protein and activates sigma 54-dependent flagellar gene promoters. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Y. Ohya,et al.  Transcriptional analysis of the flagellar regulon of Salmonella typhimurium , 1990, Journal of bacteriology.

[78]  R. Weiner,et al.  Hyphomonas species metabolise amino acids using Krebs cycle enzyme , 1990 .

[79]  J. Smit,et al.  Characterization of the Adhesive Holdfast of Marine and Freshwater Caulobacters , 1988, Applied and environmental microbiology.

[80]  T. Leisinger,et al.  Methyl Chloride: Naturally Occurring Toxicant and C-1 Growth Substrate , 1986 .

[81]  R. Weiner,et al.  Notes: Genus Hyphomonas Pongratz 1957 nom. rev. emend., Hyphomonas polymorpha Pongratz 1957 nom. rev. emend., and Hyphomonas neptunium (Leifson 1964) comb. nov. emend. (Hyphomicrobium neptunium) , 1984 .

[82]  R. Baier,et al.  Surface Microfouling During the Induction Period , 1983 .

[83]  R. Weiner,et al.  Modulation of Adenylate Energy Charge During the Swarmer Cycle of Hyphomicrobium neptunium , 1983, Journal of bacteriology.

[84]  J. Köhler,et al.  Oxidation of aromatic aldehydes and aliphatic secondary alcohols by Hyphomicrobium spp. , 1982 .

[85]  R. L. Moore The biology of Hyphomicrobium and other prosthecate, budding bacteria. , 1981, Annual review of microbiology.

[86]  R. Weiner,et al.  Timing of swarmer cell cycle morphogenesis and macromolecular synthesis by Hyphomicrobium neptunium in synchronous culture , 1980, Journal of bacteriology.

[87]  C. Dow,et al.  Morphogenesis and differentiation in Rhodomicrobium vannielii and other budding and prosthecate bacteria. , 1977, Bacteriological reviews.

[88]  D. Koshland,et al.  Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[89]  R. Weiner,et al.  Photomicrography of nalidixic acid treated Hyphomicrobium neptunium: inhibition of bud formation and bud separation. , 1975, Canadian journal of microbiology.

[90]  L. Shapiro,et al.  Regulation of the Caulobacter cell cycle. , 1975, Current topics in cellular regulation.

[91]  J. Adler,et al.  Negative Chemotaxis in Escherichia coli , 1974, Journal of bacteriology.

[92]  R. Weiner,et al.  Inhibition of Deoxyribonucleic Acid Synthesis and Bud Formation by Nalidixic Acid in Hyphomicrobium neptunium , 1973, Journal of bacteriology.

[93]  J. T. Staley Prosthecomicrobium and Ancalomicrobium: New Prosthecate Freshwater Bacteria , 1968, Journal of bacteriology.

[94]  J. Adler Chemotaxis in Bacteria , 1966, Science.

[95]  J. Poindexter BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP , 1964, Bacteriological reviews.

[96]  G. Zavarzin,et al.  [Budding bacteria]. , 1961, Mikrobiologiia.