Skip to main content
Log in

Interaction with Pantoea agglomerans Modulates Growth and Melanization of Sporothrix brasiliensis and Sporothrix schenckii

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Sporothrix brasiliensis and Sporothrix schenckii stand as the most virulent agents of sporotrichosis, a worldwide-distributed subcutaneous mycosis. The origin of Sporothrix virulence seems to be associated with fungal interactions with organisms living in the same environment. To assess this hypothesis, the growth of these two species in association with Pantoea agglomerans, a bacterium with a habitat similar to Sporothrix spp., was evaluated. Growth, melanization, and gene expression of the fungus were compared in the presence or absence of the bacterium in the same culture medium. Both S. brasiliensis and S. schenckii grew in contact with P. agglomerans yielding heavily melanized conidia after 5 days of incubation at 30 °C in Sabouraud agar. This increased melanin production occurred around bacterial colonies, suggesting that fungal melanization is triggered by a diffusible bacterial product, which is also supported by a similar pattern of melanin production during Sporothrix spp. growth in contact with heat-killed P. agglomerans. Growth of P. agglomerans was similar in the presence or absence of the fungus. However, the growth of S. brasiliensis and S. schenckii was initially inhibited, but further enhanced when these species were co-cultured with P. agglomerans. Moreover, fungi were able to use killed bacteria as both carbon and nitrogen sources for growth. Representational difference analysis identified overexpressed genes related to membrane transport when S. brasiliensis was co-cultured with the bacteria. The down-regulation of metabolism-related genes appears to be related to nutrient availability during bacterial exploitation. These findings can lead to a better knowledge on Sporothrix ecology and virulence.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  1. de Lima Barros MB, Almeida-Paes R, Schubach AO. Sporothrix schenckii and Sporotrichosis. Clin Microbiol Rev. 2011;24:633–54.

    Article  CAS  Google Scholar 

  2. Carlos IZ, Sassá MF, da Graça Sgarbi DB, Placeres MCP, Maia DCG. Current research on the immune response to experimental sporotrichosis. Mycopathologia. 2009;168:1–10.

    Article  CAS  PubMed  Google Scholar 

  3. Flournoy DJ, Mullins JB, McNeal RJ. Isolation of fungi from rose bush thorns. J Okla State Med Assoc. 2000;93:271–4.

    CAS  PubMed  Google Scholar 

  4. Dixon DM, Salkin IF, Duncan RA, Hurd NJ, Haines JH, Kemna ME, et al. Isolation and characterization of Sporothrix schenckii from clinical and environmental sources associated with the largest U.S. epidemic of sporotrichosis. J Clin Microbiol. 1991;29:1106–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. McGuinness SL, Boyd R, Kidd S, McLeod C, Krause VL, Ralph AP. Epidemiological investigation of an outbreak of cutaneous sporotrichosis, Northern Territory, Australia. BMC Infect Dis. 2016;16:16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mehta KIS, Sharma NL, Kanga AK, Mahajan VK, Ranjan N. Isolation of Sporothrix schenckii from the environmental sources of cutaneous sporotrichosis patients in Himachal Pradesh, India: results of a pilot study. Mycoses. 2007;50:496–501.

    Article  PubMed  Google Scholar 

  7. Córdoba S, Isla G, Szusz W, Vivot W, Hevia A, Davel G, et al. Molecular identification and susceptibility profile of Sporothrix schenckii sensu lato isolated in Argentina. Mycoses. 2018;61:441–8.

    Article  CAS  PubMed  Google Scholar 

  8. Ramírez-Soto MC, Aguilar-Ancori EG, Tirado-Sánchez A, Bonifaz A. Ecological determinants of Sporotrichosis etiological agents. J Fungi Basel Switz. 2018;4:95.

    Article  Google Scholar 

  9. Peleg AY, Hogan DA, Mylonakis E. Medically important bacterial–fungal interactions. Nat Rev Microbiol. 2010;8:340–9.

    Article  CAS  PubMed  Google Scholar 

  10. Harriott MM, Noverr MC. Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation. Antimicrob Agents Chemother. 2010;54:3746–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Boon C, Deng Y, Wang L-H, He Y, Xu J-L, Fan Y, et al. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2008;2:27–36.

    Article  CAS  PubMed  Google Scholar 

  12. Bamford CV, d’Mello A, Nobbs AH, Dutton LC, Vickerman MM, Jenkinson HF. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect Immun. 2009;77:3696–704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tampakakis E, Peleg AY, Mylonakis E. Interaction of Candida albicans with an intestinal pathogen, Salmonella enterica serovar Typhimurium. Eukaryot Cell. 2009;8:732–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Romano JD, Kolter R. PseudomonasSaccharomyces interactions: influence of fungal metabolism on bacterial physiology and survival. J Bacteriol. 2005;187:940–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Stirling FR, Evans TJ. Effects of the type III secreted pseudomonal toxin ExoS in the yeast Saccharomyces cerevisiae. Microbiol Read Engl. 2006;152:2273–85.

    Article  CAS  Google Scholar 

  16. Frases S, Chaskes S, Dadachova E, Casadevall A. Induction by Klebsiella aerogenes of a melanin-like pigment in Cryptococcus neoformans. Appl Environ Microbiol. 2006;72:1542–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Saito F, Ikeda R. Killing of Cryptococcus neoformans by Staphylococcus aureus: the role of cryptococcal capsular polysaccharide in the fungal-bacteria interaction. Med Mycol. 2005;43:603–12.

    Article  CAS  PubMed  Google Scholar 

  18. Rella A, Yang MW, Gruber J, Montagna MT, Luberto C, Zhang Y-M, et al. Pseudomonas aeruginosa inhibits the growth of Cryptococcus species. Mycopathologia. 2012;173:451–61.

    Article  CAS  PubMed  Google Scholar 

  19. Steenbergen JN, Nosanchuk JD, Malliaris SD, Casadevall A. Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect Immun. 2004;72:3478–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Almeida-Paes R, Borba-Santos LP, Rozental S, Marco S, Zancopé-Oliveira RM, da Cunha MML. Melanin biosynthesis in pathogenic species of Sporothrix. Fungal Biol Rev. 2017;31:50–9.

    Article  Google Scholar 

  21. Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. Pantoea agglomerans: a marvelous bacterium of evil and good. Part I. Deleterious effects: dust-borne endotoxins and allergens—focus on cotton dust. Ann Agric Environ Med AAEM. 2015;22:576–88.

    Article  CAS  PubMed  Google Scholar 

  22. Dutkiewicz J, Mackiewicz B, Kinga Lemieszek M, Golec M, Milanowski J. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants. Ann Agric Environ Med AAEM. 2016;23:197–205.

    Article  CAS  PubMed  Google Scholar 

  23. Opelt K, Berg C, Berg G. The bryophyte genus Sphagnum is a reservoir for powerful and extraordinary antagonists and potentially facultative human pathogens. FEMS Microbiol Ecol. 2007;61:38–53.

    Article  CAS  PubMed  Google Scholar 

  24. Sulbarán M, Pérez E, Ball MM, Bahsas A, Yarzábal LA. Characterization of the mineral phosphate-solubilizing activity of Pantoea agglomerans MMB051 isolated from an iron-rich soil in southeastern Venezuela (Bolívar State). Curr Microbiol. 2009;58:378–83.

    Article  CAS  PubMed  Google Scholar 

  25. Duerinckx JFH. Case report: subacute synovitis of the knee after a rose thorn injury: unusual clinical picture. Clin Orthop. 2008;466:3138–42.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Almeida-Paes R, de Oliveira LC, Oliveira MME, Gutierrez-Galhardo MC, Nosanchuk JD, Zancopé-Oliveira RM. Phenotypic characteristics associated with virulence of clinical isolates from the Sporothrix complex. Biomed Res Int. 2015;2015:212308.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Almeida-Paes R, Frases S, Fialho Monteiro PC, Gutierrez-Galhardo MC, Zancopé-Oliveira RM, Nosanchuk JD. Growth conditions influence melanization of Brazilian clinical Sporothrix schenckii isolates. Microbes Infect Inst Pasteur. 2009;11:554–62.

    Article  CAS  Google Scholar 

  28. Lee SS, Ha JK, Cheng K. Relative contributions of bacteria, protozoa, and fungi to in vitro degradation of orchard grass cell walls and their interactions. Appl Environ Microbiol. 2000;66:3807–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zambuzzi-Carvalho PF, Fernandes AG, Valadares MC, Tavares PDM, Nosanchuk JD, de Almeida Soares CM, et al. Transcriptional profile of the human pathogenic fungus Paracoccidioides lutzii in response to sulfamethoxazole. Med Mycol. 2015;53:477–92.

    Article  CAS  PubMed  Google Scholar 

  30. Téllez MD, Batista-Duharte A, Portuondo D, Quinello C, Bonne-Hernández R, Carlos IZ. Sporothrix schenckii complex biology: environment and fungal pathogenicity. Microbiol Read Engl. 2014;160:2352–65.

    Article  CAS  Google Scholar 

  31. Mares D, Romagnoli C, Andreotti E, Manfrini M, Vicentini CB. Synthesis and antifungal action of new tricyclazole analogues. J Agric Food Chem. 2004;52:2003–9.

    Article  CAS  PubMed  Google Scholar 

  32. Mowat E, Rajendran R, Williams C, McCulloch E, Jones B, Lang S, et al. Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett. 2010;313:96–102.

    Article  CAS  PubMed  Google Scholar 

  33. Chalupowicz L, Manulis-Sasson S, Itkin M, Sacher A, Sessa G, Barash I. Quorum-sensing system affects gall development incited by Pantoea agglomerans pv. gypsophilae. Mol Plant Microbe Interact MPMI. 2008;21:1094–105.

    Article  CAS  PubMed  Google Scholar 

  34. Rezzonico F, Smits THM, Montesinos E, Frey JE, Duffy B. Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol. 2009;9:204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Schafhauser J, Lepine F, McKay G, Ahlgren HG, Khakimova M, Nguyen D. The stringent response modulates 4-hydroxy-2-alkylquinoline biosynthesis and quorum-sensing hierarchy in Pseudomonas aeruginosa. J Bacteriol. 2014;196:1641–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Jouhten P, Ponomarova O, Gonzalez R, Patil KR. Saccharomyces cerevisiae metabolism in ecological context. FEMS Yeast Res. 2016;16:fow80.

    Article  CAS  Google Scholar 

  37. Mendes F, Sieuwerts S, de Hulster E, Almering MJH, Luttik MAH, Pronk JT, et al. Transcriptome-based characterization of interactions between Saccharomyces cerevisiae and Lactobacillus delbrueckii subsp. bulgaricus in lactose-grown chemostat cocultures. Appl Environ Microbiol. 2013;79:5949–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Song C, Schmidt R, de Jager V, Krzyzanowska D, Jongedijk E, Cankar K, et al. Exploring the genomic traits of fungus-feeding bacterial genus Collimonas. BMC Genom. 2015;16:1103.

    Article  CAS  Google Scholar 

  39. Schroeckh V, Scherlach K, Nützmann H-W, Shelest E, Schmidt-Heck W, Schuemann J, et al. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA. 2009;106:14558–63.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Cuomo CA, Rodriguez-Del Valle N, Perez-Sanchez L, Abouelleil A, Goldberg J, Young S, et al. Genome sequence of the pathogenic fungus Sporothrix schenckii (ATCC 58251). Genome Announc. 2014;2:e00446-14.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Teixeira MM, de Almeida LGP, Kubitschek-Barreira P, Alves FL, Kioshima ES, Abadio AKR, et al. Comparative genomics of the major fungal agents of human and animal Sporotrichosis: Sporothrix schenckii and Sporothrix brasiliensis. BMC Genom. 2014;15:943.

    Article  Google Scholar 

  42. Baidyaroy D, Brosch G, Ahn JH, Graessle S, Wegener S, Tonukari NJ, et al. A gene related to yeast HOS2 histone deacetylase affects extracellular depolymerase expression and virulence in a plant pathogenic fungus. Plant Cell. 2001;13:1609–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Shah AH, Singh A, Dhamgaye S, Chauhan N, Vandeputte P, Suneetha KJ, et al. Novel role of a family of major facilitator transporters in biofilm development and virulence of Candida albicans. Biochem J. 2014;460:223–35.

    Article  CAS  PubMed  Google Scholar 

  44. Liu Y, He Q, Cheng P. Photoreception in Neurospora: a tale of two White Collar proteins. Cell Mol Life Sci CMLS. 2003;60:2131–8.

    Article  CAS  PubMed  Google Scholar 

  45. Kim H, Kim H-K, Lee S, Yun S-H. The white collar complex is involved in sexual development of Fusarium graminearum. PLoS ONE. 2015;10:e0120293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiol Read Engl. 2004;150:3561–9.

    Article  CAS  Google Scholar 

  47. Pruss S, Fetzner R, Seither K, Herr A, Pfeiffer E, Metzler M, et al. Role of the Alternaria alternata blue-light receptor LreA (white-collar 1) in spore formation and secondary metabolism. Appl Environ Microbiol. 2014;80:2582–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cole CT. Conidiogenesis in pathogenic hyphomycetes. I. Sporothrix, Exophiala, Geotrichum and Microsporum. Sabouraudia. 1976;14:81–98.

    Article  CAS  PubMed  Google Scholar 

  49. Marimon R, Cano J, Gené J, Sutton DA, Kawasaki M, Guarro J. Sporothrix brasiliensis, S. globosa, and S. mexicana, three new Sporothrix species of clinical interest. J Clin Microbiol. 2007;45:3198–206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Garnaud C, Champleboux M, Maubon D, Cornet M, Govin J. Histone deacetylases and their inhibition in Candida species. Front Microbiol. 2016;7:1238.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ding S-L, Liu W, Iliuk A, Ribot C, Vallet J, Tao A, et al. The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell. 2010;22:2495–508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Osorio-Concepción M, Cristóbal-Mondragón GR, Gutiérrez-Medina B, Casas-Flores S. Histone deacetylase HDA-2 regulates Trichoderma atroviride growth, conidiation, blue light perception, and oxidative stress responses. Appl Environ Microbiol. 2017;83:e02922-16.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Behshad E, Parkin SE, Bollinger JM. Mechanism of cysteine desulfurase Slr0387 from Synechocystis sp. PCC 6803: kinetic analysis of cleavage of the persulfide intermediate by chemical reductants. Biochemistry. 2004;43:12220–6.

    Article  CAS  PubMed  Google Scholar 

  54. Takumi K, Nonaka G. Bacterial cysteine-inducible cysteine resistance systems. J Bacteriol. 2016;198:1384–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Eisenberg D, Gill HS, Pfluegl GM, Rotstein SH. Structure–function relationships of glutamine synthetases. Biochim Biophys Acta. 2000;1477:122–45.

    Article  CAS  PubMed  Google Scholar 

  56. Galbraith MD, Giddens SR, Mahanty HK, Clark B. Role of glutamine synthetase in phenazine antibiotic production by Pantoea agglomerans Eh1087. Can J Microbiol. 2004;50:877–81.

    Article  CAS  PubMed  Google Scholar 

  57. Quistgaard EM, Löw C, Guettou F, Nordlund P. Understanding transport by the major facilitator superfamily (MFS): structures pave the way. Nat Rev Mol Cell Biol. 2016;17:123–32.

    Article  CAS  PubMed  Google Scholar 

  58. Xu X, Chen J, Xu H, Li D. Role of a major facilitator superfamily transporter in adaptation capacity of Penicillium funiculosum under extreme acidic stress. Fungal Genet Biol FG B. 2014;69:75–83.

    Article  CAS  PubMed  Google Scholar 

  59. Roohparvar R, De Waard MA, Kema GHJ, Zwiers L-H. MgMfs1, a major facilitator superfamily transporter from the fungal wheat pathogen Mycosphaerella graminicola, is a strong protectant against natural toxic compounds and fungicides. Fungal Genet Biol FG B. 2007;44:378–88.

    Article  CAS  PubMed  Google Scholar 

  60. Dejos C, Régnacq M, Bernard M, Voisin P, Bergès T. The MFS-type efflux pump Flr1 induced by Yap1 promotes canthin-6-one resistance in yeast. FEBS Lett. 2013;587:3045–51.

    Article  CAS  PubMed  Google Scholar 

  61. Costa C, Dias PJ, Sá-Correia I, Teixeira MC. MFS multidrug transporters in pathogenic fungi: do they have real clinical impact? Front Physiol. 2014;5:197.

    PubMed  PubMed Central  Google Scholar 

  62. Natesan SK, Lamichchane AK, Swaminathan S, Wu W. Differential expression of ATP-binding cassette and/or major facilitator superfamily class efflux pumps contributes to voriconazole resistance in Aspergillus flavus. Diagn Microbiol Infect Dis. 2013;76:458–63.

    Article  CAS  PubMed  Google Scholar 

  63. Calabrese D, Bille J, Sanglard D. A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiol Read Engl. 2000;146(Pt 11):2743–54.

    Article  CAS  Google Scholar 

  64. Marimon R, Serena C, Gené J, Cano J, Guarro J. In vitro antifungal susceptibilities of five species of Sporothrix. Antimicrob Agents Chemother. 2008;52:732–4.

    Article  CAS  PubMed  Google Scholar 

  65. Almeida-Paes R, Brito-Santos F, Figueiredo-Carvalho MHG, Machado ACS, Oliveira MME, Pereira SA, et al. Minimal inhibitory concentration distributions and epidemiological cutoff values of five antifungal agents against Sporothrix brasiliensis. Mem Inst Oswaldo Cruz. 2017;112:376–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fernández-Silva F, Capilla J, Mayayo E, Guarro J. Modest efficacy of voriconazole against murine infections by Sporothrix schenckii and lack of efficacy against Sporothrix brasiliensis. Mycoses. 2014;57:121–4.

    Article  CAS  PubMed  Google Scholar 

  67. Zeilstra-Ryalls J, Fayet O, Georgopoulos C. The universally conserved GroE (Hsp60) chaperonins. Annu Rev Microbiol. 1991;45:301–25.

    Article  CAS  PubMed  Google Scholar 

  68. Tiwari S, Thakur R, Shankar J. Role of heat-shock proteins in cellular function and in the biology of fungi. Biotechnol Res Int. 2015;2015:132635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Casadevall A, Pirofski L. Accidental virulence, cryptic pathogenesis, martians, lost hosts, and the pathogenicity of environmental microbes. Eukaryot Cell. 2007;6:2169–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by Programa institucional de indução à ciência, tecnologia e inovação em saúde PAPES VI—CNPq/Fiocruz (Grant No. 407693/2012-2), Conselho Nacional de desenvolvimento Científico e Tecnológico (Grant Nos. 304976/2013-0, 449184/2014-5, and 305487/2015-9), Instituto de Ciência e Tecnologia de Estratégias de Interação Patógeno Hospedeiro (Grant Nos. 465771/2014-9, CNPq and FAPEG), and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (Grant No. E-26/103.157/2011).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosely Maria Zancopé-Oliveira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research Involving Human Participants and/or Animals

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

Informed Consent

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling editor: Marcia de Souza Carvalho Melhem.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Almeida-Paes, R., Brito-Santos, F., Oliveira, M.M.E. et al. Interaction with Pantoea agglomerans Modulates Growth and Melanization of Sporothrix brasiliensis and Sporothrix schenckii. Mycopathologia 184, 367–381 (2019). https://doi.org/10.1007/s11046-019-00350-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-019-00350-x

Keywords

Navigation