Variation in genome content and predatory phenotypes between sp. NC01 isolated from soil and type strain HD100 Open Access

Abstract

Defining phenotypic and associated genotypic variation among may further our understanding of how this genus attacks and kills different Gram-negative bacteria. We isolated sp. NC01 from soil. Analysis of 16S rRNA gene sequences and average amino acid identity showed that NC01 belongs to a different species than the type species . By clustering amino acid sequences from completely sequenced and comparing the resulting orthologue groups to a previously published analysis, we defined a ‘core genome’ of 778 protein-coding genes and identified four protein-coding genes that appeared to be missing only in NC01. To determine how horizontal gene transfer (HGT) may have impacted NC01 genome evolution, we performed genome-wide comparisons of nucleotide sequences, which indicated that eight NC01 genomic regions were likely acquired by HGT. To investigate how genome variation may impact predation, we compared protein-coding gene content between NC01 and the type strain HD100, focusing on genes implicated as important in successful killing of prey. Of these, NC01 is missing ten genes that may play roles in lytic activity during predation. Compared to HD100, NC01 kills fewer tested prey strains and kills ML35 less efficiently. NC01 causes a smaller log reduction in ML35, after which the prey population recovers and the NC01 population decreases. In addition, NC01 forms turbid plaques on lawns of ML35, in contrast to clear plaques formed by HD100. Linking phenotypic variation in interactions between and Gram-negative bacteria with underlying genome variation is valuable for understanding the ecological significance of predatory bacteria and evaluating their effectiveness in clinical applications.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000861
2019-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/165/12/1315.html?itemId=/content/journal/micro/10.1099/mic.0.000861&mimeType=html&fmt=ahah

References

  1. Jurkevitch E, Davidov Y. Phylogenetic diversity and evolution of predatory prokaryotes. In Jurkevitch E. editor Predatory Prokaryotes: Biology, Ecology and Evolution Springer: Berlin, Heidelberg; 2007 pp 11–56
    [Google Scholar]
  2. Chen H, Laws EA, Martin JL, Berhane T-K, Gulig PA et al. Relative contributions of Halobacteriovorax and bacteriophage to bacterial cell death under various environmental conditions. mBio 2018; 9: [View Article]
    [Google Scholar]
  3. Welsh RM, Zaneveld JR, Rosales SM, Payet JP, Burkepile DE et al. Bacterial predation in a marine host-associated microbiome. ISME J 2016; 10:1540–1544 [View Article]
    [Google Scholar]
  4. Feng S, Tan CH, Constancias F, Kohli GS, Cohen Y et al. Predation by Bdellovibrio bacteriovorus significantly reduces viability and alters the microbial community composition of activated sludge flocs and granules. FEMS Microbiol Ecol 2017; 93: [View Article]
    [Google Scholar]
  5. Dwidar M, Monnappa AK, Mitchell RJ. The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus . BMB Rep 2012; 45:71–78 [View Article]
    [Google Scholar]
  6. Kadouri DE, To K, Shanks RMQ, Doi Y. Predatory bacteria: a potential ally against multidrug-resistant gram-negative pathogens. PLoS One 2013; 8:e63397 [View Article]
    [Google Scholar]
  7. Tyson J, Elizabeth Sockett R, Sockett RE. Nature knows best: employing whole microbial strategies to tackle antibiotic resistant pathogens. Environ Microbiol Rep 2017; 9:47–49 [View Article]
    [Google Scholar]
  8. Martin MO. Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 2002; 4:467–477
    [Google Scholar]
  9. Koval SF, Hynes SH, Flannagan RS, Pasternak Z, Davidov Y et al. Bdellovibrio exovorus sp. nov., a novel predator of Caulobacter crescentus . Int J Syst Evol Microbiol 2013; 63:146–151 [View Article]
    [Google Scholar]
  10. Sockett RE. Predatory lifestyle of Bdellovibrio bacteriovorus . Annu Rev Microbiol 2009; 63:523–539 [View Article]
    [Google Scholar]
  11. Kuru E, Lambert C, Rittichier J, Till R, Ducret A et al. Fluorescent D-amino-acids reveal bi-cellular cell wall modifications important for Bdellovibrio bacteriovorus predation. Nat Microbiol 2017; 2:1648–1657 [View Article]
    [Google Scholar]
  12. Avidan O, Petrenko M, Becker R, Beck S, Linscheid M et al. Identification and characterization of differentially-regulated type IVb pilin genes necessary for predation in obligate bacterial predators. Sci Rep 2017; 7:1013 [View Article]
    [Google Scholar]
  13. Evans KJ, Lambert C, Sockett RE. Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 2007; 189:4850–4859 [View Article]
    [Google Scholar]
  14. Mahmoud KK, Koval SF. Characterization of type IV pili in the life cycle of the predator bacterium Bdellovibrio . Microbiology 2010; 156:1040–1051 [View Article]
    [Google Scholar]
  15. Lerner TR, Lovering AL, Bui NK, Uchida K, Aizawa S-ichi et al. Specialized peptidoglycan hydrolases sculpt the intra-bacterial niche of predatory Bdellovibrio and increase population fitness. PLoS Pathog 2012; 8:e1002524 [View Article]
    [Google Scholar]
  16. Dashiff A, Junka RA, Libera M, Kadouri DE. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus . J Appl Microbiol 2011; 110:431–444 [View Article]
    [Google Scholar]
  17. Jurkevitch E, Minz D, Ramati B, Barel G. Prey range characterization, ribotyping, and diversity of soil and rhizosphere Bdellovibrio spp. isolated on phytopathogenic bacteria. Appl Environ Microbiol 2000; 66:2365–2371 [View Article]
    [Google Scholar]
  18. Chanyi RM, Ward C, Pechey A, Koval SF. To invade or not to invade: two approaches to a prokaryotic predatory life cycle. Can J Microbiol 2013; 59:273–279 [View Article]
    [Google Scholar]
  19. Rogosky AM, Moak PL, Emmert EAB. Differential predation by Bdellovibrio bacteriovorus 109J. Curr Microbiol 2006; 52:81–85 [View Article]
    [Google Scholar]
  20. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 2004; 303:689–692 [View Article]
    [Google Scholar]
  21. Negus D, Moore C, Baker M, Raghunathan D, Tyson J et al. Predator Versus Pathogen: How Does Predatory Bdellovibrio bacteriovorus Interface with the Challenges of Killing Gram-Negative Pathogens in a Host Setting?. Annu Rev Microbiol 2017; 71:441–457 [View Article]
    [Google Scholar]
  22. Hoeniger JFM, Ladwig R, Moor H. The fine structure of "resting bodies" of Bdellovibrio sp. strain W developed in Rhodospirillum rubrum . Can J Microbiol 1972; 18:87–92 [View Article]
    [Google Scholar]
  23. Oyedara OO, Segura-Cabrera A, Guo X, Elufisan TO, Cantú González RA et al. Whole-genome sequencing and comparative genome analysis provided insight into the predatory features and genetic diversity of two Bdellovibrio species isolated from soil. Int J Genomics 2018; 2018:110 [View Article]
    [Google Scholar]
  24. Enos BG, Anthony MK, DeGiorgis JA, Williams LE. Prey range and genome evolution of Halobacteriovorax marinus predatory bacteria from an estuary. mSphere 2018; 3:e00508–00517 [View Article]
    [Google Scholar]
  25. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC et al. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 1998; 64:795–799
    [Google Scholar]
  26. Heuer H, Krsek M, Baker P, Smalla K, Wellington EM. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 1997; 63:3233–3241
    [Google Scholar]
  27. Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. error probabilities. Genome Res 1998; 8:186–194 [View Article]
    [Google Scholar]
  28. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. accuracy assessment. Genome Res 1998; 8:175–185 [View Article]
    [Google Scholar]
  29. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998; 8:195–202 [View Article]
    [Google Scholar]
  30. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  31. Pruesse E, Peplies J, Glöckner FO. Sina: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article]
    [Google Scholar]
  32. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261–5267 [View Article]
    [Google Scholar]
  33. Jurkevitch E. Isolation and classification of Bdellovibrio and Like Organisms. Current Protocols in Microbiology 20127B.1.1–7.1.7
    [Google Scholar]
  34. Koval SF. The search for hunters: culture-dependent and -independent methods for analysis of Bdellovibrio and like organisms. In Jurkevitch E. editor Predatory Prokaryotes: Biology, Ecology and Evolution Berlin, Heidelberg: Springer; 2007 pp 191–211
    [Google Scholar]
  35. Cerra J, Donohue H, Kral A, Oser M, Rostkowski L et al. Complete Genome Sequence of Pseudomonas sp. Strain NC02, Isolated from Soil. Genome Announc 2018; 6: [View Article]
    [Google Scholar]
  36. Kozlov A, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. bioRxiv 2018447110
    [Google Scholar]
  37. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016; 4:e1900v1
    [Google Scholar]
  38. Casale A, Clark S, Grasso M, Kryschuk M, Ritzer L et al. Complete Genome Sequence of Escherichia coli ML35. Genome Announc 2018; 6:e00034-18 [View Article]
    [Google Scholar]
  39. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article]
    [Google Scholar]
  40. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  41. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
    [Google Scholar]
  42. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article]
    [Google Scholar]
  43. Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L et al. Using tablet for visual exploration of second-generation sequencing data. Brief Bioinform 2013; 14:193–202 [View Article]
    [Google Scholar]
  44. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article]
    [Google Scholar]
  45. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (rast). Nucleic Acids Res 2014; 42:D206–D214 [View Article]
    [Google Scholar]
  46. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 2013; 29:2933–2935 [View Article]
    [Google Scholar]
  47. Lowe TM, Chan PP. tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–W57 [View Article]
    [Google Scholar]
  48. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article]
    [Google Scholar]
  49. Zhang Y, Sievert SM. Pan-genome analyses identify lineage- and niche-specific markers of evolution and adaptation in Epsilonproteobacteria . Front Microbiol 2014; 5: [View Article]
    [Google Scholar]
  50. Lambert C, Chang C-Y, Capeness MJ, Sockett RE. The first bite--profiling the predatosome in the bacterial pathogen Bdellovibrio. PLoS One 2010; 5:e8599 [View Article]
    [Google Scholar]
  51. Duncan MC, Gillette RK, Maglasang MA, Corn EA, Tai AK et al. High-throughput analysis of gene function in the bacterial predator Bdellovibrio bacteriovorus . mBio 2019; 10:e01040–19 [View Article]
    [Google Scholar]
  52. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. Blast ring image generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article]
    [Google Scholar]
  53. Lambert C, Sockett RE. Laboratory Maintenance of Bdellovibrio . Curr Protoc Microbiol 2008; 9:7B.2.1–7.2.7 [View Article]
    [Google Scholar]
  54. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 1994; 44:846–849 [View Article]
    [Google Scholar]
  55. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 2006; 33:152–155
    [Google Scholar]
  56. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comput Biol 2015; 11:e1004095 [View Article]
    [Google Scholar]
  57. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N et al. InterProScan: protein domains identifier. Nucleic Acids Res 2005; 33:W116–W120 [View Article]
    [Google Scholar]
  58. Ma D, Cook DN, Alberti M, Pon NG, Nikaido H et al. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli . Mol Microbiol 1995; 16:45–55 [View Article]
    [Google Scholar]
  59. Aoki SK, Malinverni JC, Jacoby K, Thomas B, Pamma R et al. Contact-Dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 2008; 70:323–340 [View Article]
    [Google Scholar]
  60. Gophna U, Charlebois RL, Doolittle WF. Ancient lateral gene transfer in the evolution of Bdellovibrio bacteriovorus . Trends Microbiol 2006; 14:64–69 [View Article]
    [Google Scholar]
  61. Pan A, Chanda I, Chakrabarti J. Analysis of the genome and proteome composition of Bdellovibrio bacteriovorus: indication for recent prey-derived horizontal gene transfer. Genomics 2011; 98:213–222 [View Article]
    [Google Scholar]
  62. Hobley L, Lerner TR, Williams LE, Lambert C, Till R et al. Genome analysis of a simultaneously predatory and prey-independent, novel Bdellovibrio bacteriovorus from the River Tiber, supports in silico predictions of both ancient and recent lateral gene transfer from diverse bacteria. BMC Genomics 2012; 13:670 [View Article]
    [Google Scholar]
  63. Fratamico PM, Whiting RC. Ability of Bdellovibrio bacteriovorus 109J to lyse Gram-negative food-borne pathogenic and spoilage bacteria. J Food Prot 1995; 58:160–164 [View Article]
    [Google Scholar]
  64. Cotter TW, Thomashow MF. Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 1992; 174:6018–6024 [View Article]
    [Google Scholar]
  65. Roschanski N, Klages S, Reinhardt R, Linscheid M, Strauch E. Identification of genes essential for prey-independent growth of Bdellovibrio bacteriovorus HD100. J Bacteriol 2011; 193:1745–1756 [View Article]
    [Google Scholar]
  66. Baker M, Negus D, Raghunathan D, Radford P, Moore C et al. Measuring and modelling the response of Klebsiella pneumoniae KPC prey to Bdellovibrio bacteriovorus predation, in human serum and defined buffer. Sci Rep 2017; 7:8329 [View Article]
    [Google Scholar]
  67. Shemesh Y, Jurkevitch E. Plastic phenotypic resistance to predation by Bdellovibrio and like organisms in bacterial prey. Environ Microbiol 2004; 6:12–18 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000861
Loading
/content/journal/micro/10.1099/mic.0.000861
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

PDF

Most cited Most Cited RSS feed