Polar growth in the Alphaproteobacterial order Rhizobiales

Elongation of many rod-shaped bacteria occurs by peptidoglycan synthesis at discrete foci along the sidewall of the cells. However, within the Rhizobiales, there are many budding bacteria, in which new cell growth is constrained to a specific region. The phylogeny of the Rhizobiales indicates that this mode of zonal growth may be ancestral. We demonstrate that the rod-shaped bacterium Agrobacterium tumefaciens grows unidirectionally from the new pole generated after cell division and has an atypical peptidoglycan composition. Polar growth occurs under all conditions tested, including when cells are attached to a plant root and under conditions that induce virulence. Finally, we show that polar growth also occurs in the closely related bacteria Sinorhizobium meliloti, Brucella abortus, and Ochrobactrum anthropi. We find that unipolar growth is an ancestral and conserved trait among the Rhizobiales, which includes important mutualists and pathogens of plants and animals.

[1]  Jay X. Tang,et al.  Surface contact stimulates the just‐in‐time deployment of bacterial adhesins , 2012, Molecular microbiology.

[2]  Pamela J. B. Brown,et al.  Polarity and the diversity of growth mechanisms in bacteria. , 2011, Seminars in cell & developmental biology.

[3]  R. Lal,et al.  Rhizobium rosettiformans sp. nov., isolated from a hexachlorocyclohexane dump site, and reclassification of Blastobacter aggregatus Hirsch and Muller 1986 as Rhizobium aggregatum comb. nov. , 2011, International journal of systematic and evolutionary microbiology.

[4]  J. T. Staley,et al.  Reclassification of the polyphyletic genus Prosthecomicrobium to form two novel genera, Vasilyevaea gen. nov. and Bauldia gen. nov. with four new combinations: Vasilyevaea enhydra comb. nov., Vasilyevaea mishustinii comb. nov., Bauldia consociata comb. nov. and Bauldia litoralis comb. nov. , 2010, International journal of systematic and evolutionary microbiology.

[5]  K. Flärdh Cell polarity and the control of apical growth in Streptomyces. , 2010, Current opinion in microbiology.

[6]  Constantin N. Takacs,et al.  MreB Drives De Novo Rod Morphogenesis in Caulobacter crescentus via Remodeling of the Cell Wall , 2009, Journal of bacteriology.

[7]  C. Fuqua,et al.  Mechanisms and regulation of polar surface attachment in Agrobacterium tumefaciens. , 2009, Current opinion in microbiology.

[8]  W. Margolin,et al.  Sculpting the Bacterial Cell , 2009, Current Biology.

[9]  Hajime Kobayashi,et al.  Sinorhizobium meliloti CpdR1 is critical for co‐ordinating cell cycle progression and the symbiotic chronic infection , 2009, Molecular microbiology.

[10]  M. Newman,et al.  Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. , 2008, Chemistry & biology.

[11]  M. de Pedro,et al.  Peptidoglycan structure and architecture. , 2008, FEMS microbiology reviews.

[12]  M. de Pedro,et al.  Morphogenesis of rod-shaped sacculi. , 2008, FEMS microbiology reviews.

[13]  J. Suh,et al.  Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. , 2008, Microbiology.

[14]  François Taddei,et al.  Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation , 2008, Proceedings of the National Academy of Sciences.

[15]  L. M. Mateos,et al.  DivIVA Is Required for Polar Growth in the MreB-Lacking Rod-Shaped Actinomycete Corynebacterium glutamicum , 2008, Journal of bacteriology.

[16]  C. Thompson,et al.  Antigen 84, an Effector of Pleiomorphism in Mycobacterium smegmatis , 2007, Journal of bacteriology.

[17]  C. Sibley,et al.  A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. , 2007, Microbiology.

[18]  M. Madiraju,et al.  Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase , 2006, Molecular microbiology.

[19]  P. van Berkum,et al.  Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). , 2006, Systematic and applied microbiology.

[20]  Shengchang Su,et al.  Lon protease of the alpha-proteobacterium Agrobacterium tumefaciens is required for normal growth, cellular morphology and full virulence. , 2006, Microbiology.

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

[22]  C. Fuqua,et al.  The FNR‐type transcriptional regulator SinR controls maturation of Agrobacterium tumefaciens biofilms , 2004, Molecular microbiology.

[23]  M. de Pedro,et al.  Restricted Mobility of Cell Surface Proteins in the Polar Regions of Escherichia coli , 2004, Journal of bacteriology.

[24]  L. M. Mateos,et al.  Involvement of DivIVA in the morphology of the rod-shaped actinomycete Brevibacterium lactofermentum. , 2003, Microbiology.

[25]  K. Flärdh Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2) , 2003, Molecular microbiology.

[26]  J. Errington,et al.  Control of Cell Morphogenesis in Bacteria Two Distinct Ways to Make a Rod-Shaped Cell , 2003, Cell.

[27]  M. de Pedro,et al.  Branching of Escherichia coli Cells Arises from Multiple Sites of Inert Peptidoglycan , 2003, Journal of bacteriology.

[28]  J. Vandenhaute,et al.  Plasticity of a transcriptional regulation network among alpha‐proteobacteria is supported by the identification of CtrA targets in Brucella abortus , 2002, Molecular microbiology.

[29]  L. Shapiro,et al.  The CcrM DNA Methyltransferase of Agrobacterium tumefaciens Is Essential, and Its Activity Is Cell Cycle Regulated , 2001, Journal of bacteriology.

[30]  R. B. Jensen,et al.  The Brucella abortus CcrM DNA Methyltransferase Is Essential for Viability, and Its Overexpression Attenuates Intracellular Replication in Murine Macrophages , 2000, Journal of bacteriology.

[31]  M. de Pedro,et al.  Murein segregation in Escherichia coli , 1997, Journal of bacteriology.

[32]  W. Margolin,et al.  Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti , 1997, Journal of bacteriology.

[33]  B. Glauner Separation and quantification of muropeptides with high-performance liquid chromatography. , 1988, Analytical biochemistry.

[34]  U. Schwarz,et al.  The composition of the murein of Escherichia coli. , 1988, The Journal of biological chemistry.

[35]  Marc Van Montagu,et al.  Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens , 1985, Nature.

[36]  S. Fukui,et al.  Unidirectional Growth and Branch Formation of a Morphological Mutant, Agrobacterium tumefaciens , 1974, Journal of bacteriology.

[37]  S. Fukui,et al.  Isolation of Morphological Mutants of Agrobacterium tumefaciens , 1972, Journal of bacteriology.

[38]  W. Wade,et al.  Bergey’s Manual of Systematic Bacteriology , 2012 .

[39]  M. Starr,et al.  Immunoferritin labeling shows de novo synthesis of surface components in buds of a prokaryote belonging to morphotype IV of theBlastocaulis-Planctomyces group , 2005, Current Microbiology.

[40]  Y. Trotsenko,et al.  Reclassification of 'Blastobacter viscosus' 7d and 'Blastobacter aminooxidans' 14a as Xanthobacter viscosus sp. nov. and Xanthobacter aminoxidans sp. nov. , 2003, International journal of systematic and evolutionary microbiology.

[41]  G. Garrity Bergey's Manual of systematic bacteriology , 2001 .