Skip to main content

Advertisement

SpringerLink
Log in

Inheritance of Pantoea type III secretion systems through both vertical and horizontal transfer

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The type III secretion system (T3SS) is an extracellular apparatus used by many Gram-negative bacteria to deliver effector proteins directly into plant and animal cells, thereby facilitating host-specific association. Strains of the enterobacterial genus, Pantoea, have been isolated from a wide variety of hosts, including plants, insects, and humans, yet it is unclear whether the T3SS may be involved in these associations. In this study, we use comparative genomics and phylogenetic methods to examine the origin and distribution of T3SSs in 35 sequenced environmental and clinical strains of Pantoea. We began our analysis by examining the distribution of the previously characterized plant cell-specific PSI-1 and animal cell-specific PSI-2 of the plant pathogenic Pantoea stewartii subsp. stewartii DC283 (PstDC283), and showed that both had a somewhat limited distribution. Our analysis, however, identified two variants of a unique plant cell-specific T3SS (PSI-1a and PSI-1b) in six Pantoea strains, including a clinical isolate. Our genome analysis of PstDC283 also identified a third T3SS that we named PSI-3, which has a similar genetic content and organization to the Salmonella, animal cell-specific SPI-2 system. Phylogenetic analysis of all three systems suggests that the PSI-1 system has been inherited vertically, whereas the newly identified PSI-1a and PSI-1b systems have been acquired independently from other genera within the Enterobacteriaceae. PSI-2 appears to have been acquired horizontally as far back as the Erwinia/Pantoea common ancestor, with evidence of more recent horizontal acquisition of the PSI-3 system. Our results suggest that Pantoea is a relatively old plant pathogen that has lost and subsequently regained different plant-associated T3SSs. This work has broad implications for understanding the host-associating capacity of Pantoea strains, and reveals the propensity for Pantoea isolates to exchange pathogenicity determinants with human-pathogenic members of the Enterobacteriaceae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alfano JR, Collmer A (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179(18):5655–5662

    PubMed Central  CAS  PubMed  Google Scholar 

  • Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    Article  CAS  PubMed  Google Scholar 

  • Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T, van Dijk K, Collmer A (2000) The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci 97(9):4856–4861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aly NY, Salmeen HN, Lila RA, Nagaraja PA (2008) Pantoea agglomerans bloodstream infection in preterm neonates. Med Princ Pract 17(6):500–503

    Article  PubMed  Google Scholar 

  • Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl Environ Microbiol 64(10):3740–3747

    PubMed Central  CAS  PubMed  Google Scholar 

  • Badel JL, Shimizu R, Oh HS, Collmer A (2006) A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol Plant Microbe Interact 19(2):99–111

    Article  CAS  PubMed  Google Scholar 

  • Bicudo EL, Macedo VO, Carrara MA, Castro FF, Rage RI (2007) Nosocomial outbreak of Pantoea agglomerans in a pediatric urgent care center. Braz J Infect Dis 11(2):281–284

    Article  PubMed  Google Scholar 

  • Boureau T, ElMaarouf-Bouteau H, Garnier A, Brisset MN, Perino C, Pucheu I, Barny MA (2006) DspA/E, a type III effector essential for Erwinia amylovora pathogenicity and growth in planta, induces cell death in host apple and nonhost tobacco plants. Mol Plant Microbe Interact 19(1):16–24

    Article  CAS  PubMed  Google Scholar 

  • Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T (2008) Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31(6–8):447–460

    Article  CAS  PubMed  Google Scholar 

  • Brady CL, Venter SN, Cleenwerck I, Vandemeulebroecke K, De Vos P, Coutinho TA (2010) Transfer of Pantoea citrea, Pantoea punctata and Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov and Tatumella terrea comb. nov and description of Tatumella morbirosei sp nov. Int J Syst Evol Microbiol 60:484–494

    Article  CAS  PubMed  Google Scholar 

  • Buttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol and Mol Biol Rev 76(2):262–310

    Article  Google Scholar 

  • Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA (2010) Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc Locus are common leaf colonizers equipped with an atypical type III secretion system. Mol Plant Microbe Interact 23(2):198–210

    Article  CAS  PubMed  Google Scholar 

  • Cornelis GR (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158(3):401–408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4(11):811–825

    Article  CAS  PubMed  Google Scholar 

  • Correa VR, Majerczak DR, Ammar E-D, Merighi M, Pratt RC, Hogenhout SA, Coplin DL, Redinbaugh MG (2012) The bacterium Pantoea stewartii uses two different type III secretion systems to colonize its plant host and insect vector. Appl Environ Microbiol 78(17):6327–6336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 45(6):1989–1992

    Article  PubMed Central  PubMed  Google Scholar 

  • Dale C, Young SA, Haydon DT, Welburn SC (2001) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci 98(4):1883–1888

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dale C, Jones T, Pontes M (2005) Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius. Mol Biol Evol 22(3):758–766

    Article  CAS  PubMed  Google Scholar 

  • De Champs C, Le Seaux S, Dubost JJ, Boisgard S, Sauvezie B, Sirot J (2000) Isolation of Pantoea agglomerans in two cases of septic monoarthritis after plant thorn and wood sliver injuries. J Clin Microbiol 38(1):460–461

    PubMed Central  PubMed  Google Scholar 

  • De Maayer P, Chan W, Blom J, Venter S, Duffy B, Smits T, Coutinho T (2012) The large universal Pantoea plasmid LPP-1 plays a major role in biological and ecological diversification. BMC Genom. doi:10.1186/1471-2164-13-625

    Google Scholar 

  • DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci 101(26):9927–9932

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diallo MD, Monteil CL, Vinatzer BA, Clarke CR, Glaux C, Guilbaud C, Desbiez C, Morris CE (2012) Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic. ISME J 6(7):1325–1335

    Article  PubMed Central  CAS  Google Scholar 

  • Dieye Y, Ameiss K, Mellata M, Curtiss R (2009) The Salmonella Pathogenicity Island (SPI) 1 contributes more than SPI2 to the colonization of the chicken by Salmonella enterica serovar Typhimurium. BMC Microbiol 9(1):3

    Article  PubMed Central  PubMed  Google Scholar 

  • Duan J, Yi T, Lu Z, Shen D, Feng Y (2007) Rice endophyte Pantoea agglomerans YS19 forms multicellular symplasmata via cell aggregation. FEMS Microbiol Lett 270(2):220–226

    Article  CAS  PubMed  Google Scholar 

  • Duerinckx JF (2008) Case report: subacute synovitis of the knee after a rose thorn injury: unusual clinical picture. Clin Orthop Relat Res 466(12):3138–3142

    Article  PubMed Central  PubMed  Google Scholar 

  • Flatauer FE, Khan MA (1978) Septic arthritis caused by Enterobacter agglomerans. Arch Intern Med 138(5):788

    Article  CAS  PubMed  Google Scholar 

  • Foultier B, Troisfontaines P, Vertommen D, Marenne MN, Rider M, Parsot C, Cornelis GR (2003) Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system. Infect Immun 71(1):242–253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frederick RD, Ahmad M, Majerczak DR, Arroyo-Rodriguez AS, Manulis S, Coplin DL (2001) Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. Mol Plant Microbe Interact 14(10):1213–1222

    Article  CAS  PubMed  Google Scholar 

  • Galan J, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284(5418):1322–1328

    Article  CAS  PubMed  Google Scholar 

  • Gaudriault S, Malandrin L, Paulin JP, Barny MA (1997) DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol 26(5):1057–1069

    Article  CAS  PubMed  Google Scholar 

  • Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, De Ley J (1989) Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and Description of Pantoea dispersa sp. nov. Int J Sys Bacteriol 39(3):337–345

    Article  Google Scholar 

  • Gitaitis R, Gay J (1997) First report of a leaf blight, seed stalk rot, and bulb decay of onion by Pantoea ananas in Georgia. Plant Dis 81(9):1096

    Article  Google Scholar 

  • Ham JH, Majerczak DR, Arroyo-Rodriguez AS, Mackey DM, Coplin DL (2006) WtsE, an AvrE-family effector protein from Pantoea stewartii subsp. stewartii, causes disease-associated cell death in corn and requires a chaperone protein for stability. Mol Plant Microbe Interact 19(10):1092–1102

    Article  CAS  PubMed  Google Scholar 

  • Ham JH, Majerczak D, Ewert S, Sreerekha MV, Mackey D, Coplin D (2008) WtsE, an AvrE-family type III effector protein of Pantoea stewartii subsp. stewartii, causes cell death in non-host plants. Mol. Plant Pathol 9(5):633–643

    Article  CAS  Google Scholar 

  • Hensel M (2000) Salmonella pathogenicity island 2. Mol Microbiol 36(5):1015–1023

    Article  CAS  PubMed  Google Scholar 

  • Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62(2):379–433

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hurst MRH, Becher SA, Young SD, Nelson TL, Glare TR (2011) Yersinia entomophaga sp. nov., isolated from the New Zealand grass grub Costelytra zealandica. Int J Sys Evol Microbiol 61:844–849

    Article  CAS  Google Scholar 

  • Kido K, Adachi R, Hasegawa M, Yano K, Hikichi Y, Takeuchi S, Atsuchi T, Takikawa Y (2008) Internal fruit rot of netted melon caused by Pantoea ananatis (Erwinia ananas) in Japan. J Gen Plant Pathol 74(4):302–312

    Article  CAS  Google Scholar 

  • Kirzinger MWB, Stavrinides J (2012) Host specificity determinants as a genetic continuum. Trends Microbiol 20(2):88–93

    Article  CAS  PubMed  Google Scholar 

  • Kirzinger MWB, Nadarasah G, Stavrinides J (2011) Insights into cross-kingdom plant pathogenic bacteria. Genes 2(4):980–997

    Article  PubMed Central  PubMed  Google Scholar 

  • Kosako Y, Sakazaki R, Yoshizaki E (1984) Yokenella regensburgei gen nov, sp-nov—a new genus and species in the family Enterobacteriaceae. Jpn J Med Sci Biol 37(3):117–124

    Article  CAS  PubMed  Google Scholar 

  • Kratz A, Greenberg D, Barki Y, Cohen E, Lifshitz M (2003) Pantoea agglomerans as a cause of septic arthritis after palm tree thorn injury; case report and literature review. Arch Dis Child 88(6):542–544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lalas KM, Erichsen D (2010) Sporadic Pantoea agglomerans bacteremia in a near-term female: case report and review of literature. Jpn J Infect Dis 63(4):290–291

    PubMed  Google Scholar 

  • Lawrence JG, Ochman H (1997) Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44(4):383–397

    Article  CAS  PubMed  Google Scholar 

  • Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, Dangl JL, Greenberg JT, Mansfield JW, Guttman DS (2005) Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact 18(4):275–282

    Article  CAS  PubMed  Google Scholar 

  • Lo YC, Chuang YW, Lin YH (2011) Yokenella regensburgei in an immunocompromised host: a case report and review of the literature. Infection 39(5):485–488

    Article  PubMed  Google Scholar 

  • Lostroh CP, Lee CA (2001) The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect 3(14–15):1281–1291

    Article  CAS  PubMed  Google Scholar 

  • Ma W, Dong FFT, Stavrinides J, Guttman DS (2006) Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet 2(12):2131–2142

    Article  CAS  Google Scholar 

  • Manulis S, Barash I (2003) Pantoea agglomerans pvs. gypsophilae and betae, recently evolved pathogens? Mol Plant Pathol 4(5):307–314

    Article  CAS  PubMed  Google Scholar 

  • Marie C, Broughton WJ, Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 4(4):336–342

    Article  CAS  PubMed  Google Scholar 

  • Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509–531

    Article  CAS  PubMed  Google Scholar 

  • Nadarasah G, Stavrinides J (2014) Quantitative evaluation of the host colonizing capabilities of the enteric bacterium, Pantoea, using plant and insect hosts. Microbiol 160:602–615

    Article  CAS  Google Scholar 

  • Nissan G, Manulis-Sasson S, Weinthal D, Mor H, Sessa G, Barash I (2006) The type III effectors HsvG and HsvB of gall-forming Pantoea agglomerans determine host specificity and function as transcriptional activators. Mol Microbiol 61(5):1118–1131

    Article  CAS  PubMed  Google Scholar 

  • Perry RD, Fetherston JD (1997) Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev 10(1):35–66

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rezzonico F, Smits TH, Montesinos E, Frey JE, Duffy B (2009) Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol 9:204

    Article  PubMed Central  PubMed  Google Scholar 

  • Roden JA, Belt B, Ross JB, Tachibana T, Vargas J, Mudgett MB (2004) A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc Natl Acad Sci 101(47):16624–16629

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sarkar SF, Guttman DS (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 70(4):1999–2012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sawada H, Suzuki F, Matsuda I, Saitou N (1999) Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. J Mol Evol 49(5):627–644

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Li WH (1987) The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucl Acids Res 15(3):1281–1295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith DDN, Kirzinger MWB, Stavrinides J (2013a) Draft genome sequence of the antibiotic-producing epiphytic isolate Pantoea ananatis BRT175. Genome Announc 1(6):e00902-13. doi:10.1128/genomeA.00902-13

    Article  PubMed Central  PubMed  Google Scholar 

  • Smith DDN, Kirzinger MWB, Stavrinides J (2013b) Draft genome sequence of the antibiotic-producing cystic fibrosis isolate Pantoea agglomerans Tx10. Genome Announc 1(5):e00904-13. doi:10.1128/genomeA.00904-13

    Article  PubMed Central  PubMed  Google Scholar 

  • Stavrinides J (2009) Origin and evolution of phytopathogenic bacteria. In: Jackson RW (ed) Plant pathogenic bacteria: genomics and molecular biology. Caister Academic Press, pp 1–35

  • Stavrinides J, McCann HC, Guttman DS (2008) Host-pathogen interplay and the evolution of bacterial effectors. Cell Microbiol 10(2):285–292

    CAS  PubMed  Google Scholar 

  • Stavrinides J, No A, Ochman H (2010) A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ Microbiol 12(1):147–155

    Article  CAS  PubMed  Google Scholar 

  • Suarez M, Russmann H (1998) Molecular mechanisms of Salmonella invasion: the type III secretion system of the pathogenicity island 1. Int Microbiol 1(3):197–204

    CAS  PubMed  Google Scholar 

  • Subtil A, Blocker A, Dautry-Varsat A (2000) Type III secretion system in Chlamydia species: identified members and candidates. Microbes Infect 2(4):367–369

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28(10):2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tardy F, Homble F, Neyt C, Wattiez R, Cornelis GR, Ruysschaert JM, Cabiaux V (1999) Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J 18(23):6793–6799

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, Hattori M, Aksoy S (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16(2):149–156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Troisfontaines P, Cornelis GR (2005) Type III secretion: more systems than you think. Physiol 20:326–339

    Article  CAS  Google Scholar 

  • Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28(6):1381–1389

    Article  CAS  PubMed  Google Scholar 

  • Volksch B, Thon S, Jacobsen ID, Gube M (2009) Polyphasic study of plant- and clinic-associated Pantoea agglomerans strains reveals indistinguishable virulence potential. Infect Genet Evol 9(6):1381–1391

    Article  PubMed  Google Scholar 

  • Walterson AM, Smith DDN, Stavrinides J (2014) Identification of a Pantoea biosynthetic cluster that directs the synthesis of an antimicrobial natural product. PLoS ONE 9(5):e96208–e96208

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the intellectual contributions of Dr. Andrew Cameron to nomenclature and naming. This work was supported by Discovery Grants from the Natural Sciences and Engineering Council to CB (#238880) and JS (#386654), and a Canada Foundation for Innovation LOF (#28591) to JS.

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Authors and Affiliations

  1. Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, SK, S4S0A2, Canada

    Morgan W. B. Kirzinger & John Stavrinides

  2. Department of Computer Science, University of Regina, 3737 Wascana Parkway, Regina, SK, S4S0A2, Canada

    Cory J. Butz

Authors
  1. Morgan W. B. Kirzinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cory J. Butz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John Stavrinides
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John Stavrinides.

Additional information

Communicated by A. M. Hirsch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 28 kb)

Supplementary material 2 (XLS 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kirzinger, M.W.B., Butz, C.J. & Stavrinides, J. Inheritance of Pantoea type III secretion systems through both vertical and horizontal transfer. Mol Genet Genomics 290, 2075–2088 (2015). https://doi.org/10.1007/s00438-015-1062-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1062-2

Keywords

Search

Navigation