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Plasmids Bring Additional Capabilities to Caulobacter Isolates

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Abstract

Caulobacter is a well-studied bacterial genus, but little is known about the plasmids that are found in some wild Caulobacter isolates. We used bioinformatic approaches to identify nine plasmids from seven different Caulobacter strains and grouped them based on their size and the similarity of their repABC, parAB, and mobAB genes. Protein pathway analysis of the genes on the K31p1 and K31p2 plasmids showed many metabolic pathways that would enhance the metabolic versatility of the host strain. In contrast, the CB4 plasmid contained 21 heavy metal resistance genes with the majority coding for proteins that enhance copper resistance. Growth assays of C. henricii CB4 demonstrated increased copper resistance and quantitative PCR showed an increase in the expression of eight heavy metal genes when induced with copper.

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References

  1. Clowes RC (1972) Molecular structure of bacterial plasmids. Bacteriol Rev 36(3):361–405

    Article  CAS  Google Scholar 

  2. Bouma JE, Lenski RE (1988) Evolution of a bacteria/plasmid association. Nat 335(6188):351–352

    Article  CAS  Google Scholar 

  3. Moreno E (1998) Genome evolution within the alpha Proteobacteria: why do some bacteria not possess plasmids and others exhibit more than one different chromosome? FEMS Microbiol Rev 22(4):255–275

    Article  CAS  Google Scholar 

  4. Shintani M, Sanchez ZK, Kimbara K (2015) Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol 6:242. https://doi.org/10.3389/fmicb.2015.00242

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cevallos MA, Cervantes-Rivera R, Gutiérrez-Ríos RM (2008) The repABC plasmid family. Plasmid 60(1):19–37. https://doi.org/10.1016/j.plasmid.2008.03.001

    Article  CAS  PubMed  Google Scholar 

  6. Pinto UM, Pappas KM, Winans SC (2012) The ABCs of plasmid replication and segregation. Nat Rev Microbiol 10(11):755–765. https://doi.org/10.1038/nrmicro2882

    Article  CAS  PubMed  Google Scholar 

  7. Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28(3):231–295

    Article  CAS  Google Scholar 

  8. Degnen ST, Newton A (1972) Chromosome replication during development in Caulobacter crescentus. J Mol Biol 64(3):671–680

    Article  CAS  Google Scholar 

  9. Laub MT, McAdams HH, Feldblyum T, Fraser CM, Shapiro L (2000) Global analysis of the genetic network controlling a bacterial cell cycle. Science 290(5499):2144–2148

    Article  CAS  Google Scholar 

  10. Ely B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204:372–384

    Article  CAS  Google Scholar 

  11. Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen J, Heidelberg JF, Alley MR, Ohta N, Maddock JR, Potocka I (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98(7):4136–4141

    Article  CAS  Google Scholar 

  12. Christen B, Abeliuk E, Collier JM, Kalogeraki VS, Passarelli B, Coller JA, Fero MJ, McAdams HH, Shapiro L (2011) The essential genome of a bacterium. Molec Syst Biol 7(1):528. https://doi.org/10.1038/msb.2011.58

    Article  CAS  Google Scholar 

  13. Scott D, Ely B (2016) Conservation of the essential genome among Caulobacter and Brevundimonas species. Curr Microbiol 72(5):503–510. https://doi.org/10.1007/s00284-015-0964-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ely B, Wilson K, Ross K, Ingram D, Lewter T, Herring J, Duncan D, Aikins A, Scott D (2019) Genome comparisons of wild isolates of Caulobacter crescentus reveal rates of inversion and horizontal gene transfer. Curr Microbiol 76(2):159–167. https://doi.org/10.1007/s00284-018-1606-x

    Article  CAS  PubMed  Google Scholar 

  15. Schoenlein PV, Ely B (1983) Plasmids and bacteriocins in Caulobacter species. J Bacteriol 153(2):1092–1094

    Article  CAS  Google Scholar 

  16. Eberhard WG (1990) Evolution in bacterial plasmids and levels of selection. Q Rev Biol 65(1):3–22

    Article  CAS  Google Scholar 

  17. Madden T (2013) The BLAST sequence analysis tool. In: The NCBI handbook [Internet]. 2nd edition National Center for Biotechnology Information (US)

  18. Okonechnikov K, Golosova O, Fursov M, Ugene Team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinform 28(8):1166–1167

    Article  Google Scholar 

  19. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365

    Article  Google Scholar 

  20. Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14(7):1394–1403

    Article  CAS  Google Scholar 

  21. Johnson RC, Ely B (1977) Isolation of spontaneously derived mutants of Caulobacter crescentus. Genet 86(1):25–32

    Article  CAS  Google Scholar 

  22. Scott D, Ely B (2015) Comparison of genome sequencing technology and assembly methods for the analysis of a GC-rich bacterial genome. Curr Microbiol 70:338–344. https://doi.org/10.1007/s00284-014-0721-6

    Article  CAS  PubMed  Google Scholar 

  23. Bartosik D, Szymanik M, Wysocka E (2001) Identification of the partitioning site within the repABC-Type Replicon of the composite Paracoccus versutus plasmid pTAV1. J Bacteriol 183(21):6234–6243

    Article  CAS  Google Scholar 

  24. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R, Machi D (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucl Acid Res 42(D1):D581–D591

    Article  CAS  Google Scholar 

  25. Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27(2–3):197–213

    Article  CAS  Google Scholar 

  26. Arguello JM, Raimunda D, Padilla-Benavides T (2013) Mechanisms of copper homeostasis in bacteria. Front Cell Infect Microbiol 3:73. https://doi.org/10.3389/fcimb.2013.00073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lawton TJ, Kenney GE, Hurley JD, Rosenzweig AC (2016) The CopC family: structural and bioinformatic insights into a diverse group of periplasmic copper binding proteins. Biochem 55(15):2278–2290. https://doi.org/10.1021/acs.biochem.6b00175

    Article  CAS  Google Scholar 

  28. Blair JM, Piddock LJ (2009) Structure, function and inhibition of RND efflux pumps in Gram-negative bacteria: an update. Curr Opin Microbiol 12(5):512–519. https://doi.org/10.1016/j.mib.2009.07.003

    Article  CAS  PubMed  Google Scholar 

  29. Inesi G, Pilankatta R, Tadini-Buoninsegni F (2014) Biochemical characterization of P-type copper ATPases. Biochem J 463(2):167–176

    Article  CAS  Google Scholar 

  30. Giachino A, Waldron KJ (2020) Copper tolerance in bacteria requires the activation of multiple accessory pathways. Molec Microbiol 114(3):377–390. https://doi.org/10.1111/mmi.14522

    Article  CAS  Google Scholar 

  31. Fang C, Philips SJ, Wu X, Chen K, Shi J, Shen L, Xu J, Feng Y, O’Halloran TV, Zhang Y (2020) CueR activates transcription through a DNA distortion mechanism. Nat Chem Biol 17:57–64. https://doi.org/10.1038/s41589-020-00653-x

    Article  CAS  PubMed  Google Scholar 

  32. Moraleda-Muñoz A, Pérez J, Extremera AL, Muñoz-Dorado J (2010) Differential regulation of six heavy metal efflux systems in the response of Myxococcus xanthus to copper. Appl Environ Microbiol 76(18):6069–6076

    Article  Google Scholar 

  33. Hassan KA, Pederick VG, Elbourne LD, Paulsen IT, Paton JC, McDevitt CA, Eijkelkamp BA (2017) Zinc stress induces copper depletion in Acinetobacter baumannii. BMC Microbiol 17(1):1–5. https://doi.org/10.1186/s12866-017-0965-y

    Article  CAS  Google Scholar 

  34. Solioz M, Odermatt A (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270(16):9217–9221

    Article  CAS  Google Scholar 

  35. Crack JC, Green J, Hutchings MI, Thomson AJ, Le Brun NE (2012) Bacterial iron–sulfur regulatory proteins as biological sensor-switches. Antioxid Redox Signal 17(9):1215–1231

    Article  CAS  Google Scholar 

  36. Stoyanov JV, Hobman JL, Brown NL (2001) CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Molec Microbiol 39(2):502–512

    Article  CAS  Google Scholar 

  37. Outten FW, Outten CE, Hale J, O’Halloran TV (2000) Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, CueR. J Biol Chem 275(40):31024–31029

    Article  CAS  Google Scholar 

  38. Whitman T, Neurath R, Perera A, Chu-Jacoby I, Ning D, Zhou J, Nico P, Pett-Ridge J, Firestone M (2018) Microbial community assembly differs across minerals in a rhizosphere microcosm. Environ Microbiol 20(12):4444–4460. https://doi.org/10.1111/1462-2920.14366

    Article  CAS  PubMed  Google Scholar 

  39. Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71. https://doi.org/10.1016/j.btre.2016.12.006

    Article  Google Scholar 

  40. Qi X, Liu R, Chen M, Li Z, Qin T, Qian Y, Zhao S, Liu M, Zeng Q, Shen J (2019) Removal of copper ions from water using polysaccharide-constructed hydrogels. Carbohydr Polym 209:101–110. https://doi.org/10.1016/j.carbpol.2019.01.015

    Article  CAS  PubMed  Google Scholar 

  41. Deschatre M, Ghillebaert F, Guezennec J, Colin CS (2013) Sorption of copper (II) and silver (I) by four bacterial exopolysaccharides. Appl Biochem Biotechnol 171(6):1313–1327. https://doi.org/10.1007/s12010-013-0343-7

    Article  CAS  PubMed  Google Scholar 

  42. Vodyanitskii YN (2010) Iron hydroxides in soils: a review of publications. Eurasian Soil Sci 43(11):1244–1254

    Article  Google Scholar 

  43. Ash K, Brown T, Watford T, Scott LE, Stephens C, Ely B (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biol 4(10):140128. https://doi.org/10.1098/rsob.140128

    Article  PubMed  PubMed Central  Google Scholar 

  44. Petersen J, Brinkmann H, Pradella S (2009) Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 10:2627–2638. https://doi.org/10.1111/j.1462-2920.2009.01987

    Article  Google Scholar 

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Funding

This work was funded in part by Grant R25GM076277 to BE from the National Institutes of Health.

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  1. Taylor Carter

    Present address: Deptartment of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC, 29208, USA

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  1. Department of Biological Sciences, University of South Carolina, Columbia, SC, 29208, USA

    Taylor Carter & Bert Ely

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TC performed the experimental work. Both BE and TC contributed to the design of the study, the interpretation of results, and the writing of the manuscript.

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Correspondence to Taylor Carter.

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Supplementary Information

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Supplementary file1 (DOCX 13 kb)

284_2021_2742_MOESM2_ESM.tif

Supplementary file2 (TIF 90714 kb) Supplementary 2. Mauve alignment of the medium-sized plasmids. The red areas represent regions of nucleotide similarity between plasmids which includes replication, mobility, and partitioning genes in the same gene order for each plasmid.

284_2021_2742_MOESM3_ESM.tif

Supplementary file3 (TIF 87311 kb) Supplementary 3. Mauve alignment of the large-sized plasmids. Colored areas are areas of homology as determine by Mauve. The pink areas contain the repC gene, the purple areas contain parB gene, and the teal areas contain repAB, mobA, and parA genes. The dark purple areas contain fatty acid synthesis genes, while the hunter green areas contain branched-chain amino acid synthesis genes.

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Supplementary file5 (DOCX 12 kb)

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Carter, T., Ely, B. Plasmids Bring Additional Capabilities to Caulobacter Isolates. Curr Microbiol 79, 45 (2022). https://doi.org/10.1007/s00284-021-02742-z

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  • DOI: https://doi.org/10.1007/s00284-021-02742-z