1887

Abstract

In recent years, the genus has emerged as a pathogen in healthcare-related infections and has became stablished as an opportunistic pathogen.

Little is known about the pathogenesis induced by genus.

To evaluate the cytotoxic effects of genus , its ability to adhere to lung human cells and the ability of environmental and clinical strains of to induce pneumonia in mice.

Environmental and clinical isolates of were examined for their cytotoxic effects on the Calu-3 cell lineage. Cytotoxic activity of secretome was tested using MTT/neutral red assays and cell morphology analysis. adhesion on Calu-3 cells was assessed using bright-field microscopy and cell-associated bacteria were counted. A mouse model of acute lung infection was done using a clinical and an environmental strain. Adult male mice were used, and the pneumonia was inducted by intra-tracheal inoculation of 10 or 10 bacteria. Mice weight variations were evaluated at the end of the experiment. Bronchoalveolar lavage was collected and evaluated for total and differential cytology. A histological examination of lungs was performed giving a histological score.

The secretomes of all the strains induced morphological alterations in cells, but only SmR1 were cytotoxic in MTT and neutral red assays. Clinical strains of AU14459 and subsp. AU11883 exhibited low adherence to lung cells, while SmR1 was non-adhesive. Following intratracheal inoculation, mice treated with 10 c.f.u. of the SmR1 and AU11883 strains lost 18 and 6% of their weight over 7 days, respectively, and presented moderate clinical signs. Infected mice showed inflammatory cell infiltration in the perivascular and peribroncheal/peribronchiolar spaces. Bronchoalveolar fluid of mice inoculated with SmR1 10 c.f.u. presented an increase in total leucocyte cells and in neutrophils population.

These and results provide insights into how some strains cause infection in humans, providing a basis for the characterization of pathogenesis studies on this emerging infectious agent.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001343
2021-04-08
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/4/jmm001343.html?itemId=/content/journal/jmm/10.1099/jmm.0.001343&mimeType=html&fmt=ahah

References

  1. Baldani JI, Baldani VLD, Seldin L, Döbereiner J. Characterization of Herbaspirillum seropedicae gen. nov. sp. nov. a root- associated nitrogen-fixing bacterium. Int J Syst Bacteriol 1986; 36:8
    [Google Scholar]
  2. Dobritsa AP, Reddy MCS, Samadpour M. Reclassification of Herbaspirillum putei as a later heterotypic synonym of Herbaspirillum huttiense, with the description of H. huttiense subsp. huttiense subsp. nov. and H. huttiense subsp. putei subsp. nov., comb. nov., and description of Herbaspirillum aquaticum sp. nov. Int J Syst Evol Microbiol 2010; 60:1418–1426 [View Article][PubMed]
    [Google Scholar]
  3. Carro L, Rivas R, León-Barrios M, González-Tirante M, Velázquez E et al. Herbaspirillum canariense sp. nov., Herbaspirillum aurantiacum sp. nov. and Herbaspirillum soli sp. nov., isolated from volcanic mountain soil, and emended description of the genus Herbaspirillum . Int J Syst Evol Microbiol 2012; 62:1300–1306 [View Article][PubMed]
    [Google Scholar]
  4. Ding L, Yokota A. Proposals of Curvibacter gracilis gen. nov., sp. nov. and Herbaspirillum putei sp. nov. for bacterial strains isolated from well water and reclassification of [Pseudomonas] huttiensis, [Pseudomonas] lanceolata, [Aquaspirillum] delicatum and [Aquaspirillum] autotrophicum as Herbaspirillum huttiense comb. nov., Curvibacter lanceolatus comb. nov., Curvibacter delicatus comb. nov. and Herbaspirillum autotrophicum comb. nov. Int J Syst Evol Microbiol 2004; 54:2223–2230 [View Article][PubMed]
    [Google Scholar]
  5. Im W-T, Bae H-S, Yokota A, Lee ST. Herbaspirillum chlorophenolicum sp. nov., a 4-chlorophenol-degrading bacterium. Int J Syst Evol Microbiol 2004; 54:851–855 [View Article][PubMed]
    [Google Scholar]
  6. Kirchhof G, Eckert B, Stoffels M, Baldani JI, Reis VM et al. Herbaspirillum frisingense sp. nov., a new nitrogen-fixing bacterial species that occurs in C4-fibre plants. Int J Syst Evol Microbiol 2001; 51:157–168 [View Article][PubMed]
    [Google Scholar]
  7. Rothballer M, Schmid M, Klein I, Gattinger A, Grundmann S et al. Herbaspirillum hiltneri sp. nov., isolated from surface-sterilized wheat roots. Int J Syst Evol Microbiol 2006; 56:1341–1348 [View Article][PubMed]
    [Google Scholar]
  8. Valverde A, Velázquez E, Gutiérrez C, Cervantes E, Ventosa A et al. Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris . Int J Syst Evol Microbiol 2003; 53:1979–1983 [View Article][PubMed]
    [Google Scholar]
  9. Jung S-Y, Lee M-H, Oh T-K, Yoon J-H. Herbaspirillum rhizosphaerae sp. nov., isolated from rhizosphere soil of Allium victorialis var. platyphyllum. Int J Syst Evol Microbiol 2007; 57:2284–2288 [View Article][PubMed]
    [Google Scholar]
  10. Baldani JI, Pot B, Kirchhof G, Falsen E, Baldani VL et al. Emended description of Herbaspirillum; inclusion of [Pseudomonas] rubrisubalbicans, a milk plant pathogen, as Herbaspirillum rubrisubalbicans comb. nov.; and classification of a group of clinical isolates (EF group 1) as Herbaspirillum species 3. Int J Syst Bacteriol 1996; 46:802–810 [View Article][PubMed]
    [Google Scholar]
  11. Liu X, Zhou J, Tian J, Cheng W, Wang X. Herbaspirillum camelliae sp. nov., a novel endophytic bacterium isolated from Camellia sinensis L. Arch Microbiol 2020; 202:1801–1807
    [Google Scholar]
  12. Bastián F, Cohen A, Piccoli P et al. Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regulation 1998; 24:7–11
    [Google Scholar]
  13. Tan MJ, Oehler RL. Lower extremity cellulitis and bacteremia with Herbaspirillum seropedicae associated with aquatic exposure in a patient with cirrhosis. Infect Di Clin Pract 2005; 13:277–279
    [Google Scholar]
  14. Ziga ED, Druley T, Burnham CA. Herbaspirillum species bacteremia in a pediatric oncology patient. J Clin Microbiol 2010; 48:4320–4321
    [Google Scholar]
  15. Regunath H, Kimball J, Smith LP, Salzer W. Severe community-acquired pneumonia with bacteremia caused by Herbaspirillum aquaticum or Herbaspirillum huttiense in an immune-competent adult. J Clin Microbiol 2015; 53:3086–3088
    [Google Scholar]
  16. Coenye T, Goris J, Spilker T, Vandamme P, LiPuma JJ. Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 2002; 40:2062–2069
    [Google Scholar]
  17. Spilker T, Uluer AZ, Marty FM et al. Recovery of Herbaspirillum species from persons with cystic fibrosis. J Clin Microbiol 2008; 46:2774–2777
    [Google Scholar]
  18. Chemaly RF, Dantes R, Shah DP et al. Cluster and sporadic cases of Herbaspirillum species infections in patients with cancer. Clin Infect Dis 2015; 60:48–54
    [Google Scholar]
  19. Liu C, Kwon MJ, Kim M, Byun JH, Yong D et al. Septicemia caused by Herbaspirillum huttiense secondary to pneumonia. Ann Lab Med 2019; 39:340–342
    [Google Scholar]
  20. Dhital R, Paudel A, Bohra N, Shin AK. Herbaspirillum infection in humans: a case report and review of literature. Case Rep Infect Dis 2020; 2020:9545243
    [Google Scholar]
  21. Faoro H, Oliveira WK, Weiss VA et al. Genome comparison between clinical and environmental strains of Herbaspirillum seropedicae reveals a potential new emerging bacterium adapted to human hosts. BMC Genomics 2019; 20:630
    [Google Scholar]
  22. Tetz V, Tetz G. Draft genome sequence of the uropathogenic Herbaspirillum frisingense strain ureolyticus VT-16-41. Genome Announc 2017; 5:e00279–17
    [Google Scholar]
  23. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65:55–63
    [Google Scholar]
  24. Marty KB, Williams CL, Guynn LJ, Benedik MJ, Blanke SR. Characterization of a cytotoxic factor in culture filtrates of Serratia marcescens . Infect Immun 2002; 70:1121–1128
    [Google Scholar]
  25. Borenfreund E, Puerner JA. Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol Lett 1985; 24:119–124
    [Google Scholar]
  26. Scaletsky IC, Silva ML, Trabulsi LR. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 1984; 45:534–536
    [Google Scholar]
  27. Grey PA, Kirov SM. Adherence to HEp-2 cells and enteropathogenic potential of Aeromonas spp. Epidemiol Infect 1993; 110:279–287
    [Google Scholar]
  28. Brieland J, Freeman P, Kunkel R et al. Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. a murine model of human Legionnaires' disease. Am J Pathol 1994; 145:1537–1546
    [Google Scholar]
  29. Eveillard M, Soltner C, Kempf M et al. The virulence variability of different Acinetobacter baumannii strains in experimental pneumonia. J Infect 2010; 60:154–161
    [Google Scholar]
  30. Cimolai N, Taylor GP, Mah D, Morrison BJ. Definition and application of a histopathological scoring scheme for an animal model of acute Mycoplasma pneumoniae pulmonary infection. Microbiol Immunol 1992; 36:465–478
    [Google Scholar]
  31. Matute-Bello G, Winn RK, Jonas M, Chi EY, Martin TR et al. Cd95) induces alveolar epithelial cell apoptosis in vivo: implications for acute pulmonary inflammation. Am J Pathol 2001; 158:153–161
    [Google Scholar]
  32. Beck MA, Nelson HK, Shi Q et al. Selenium deficiency increases the pathology of an influenza virus infection. Faseb J 2001; 15:1481–1483
    [Google Scholar]
  33. Faul F, Erdfelder E, Lang AG. Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007; 39:175–191
    [Google Scholar]
  34. Marques AC, Paludo KS, Dallagassa CB et al. Biochemical characteristics, adhesion, and cytotoxicity of environmental and clinical isolates of Herbaspirillum spp. J Clin Microbiol 2015; 53:302–308
    [Google Scholar]
  35. Cornelis GR, Van Gijsegem F. Assembly and function of type III secretory systems. Annu Rev Microbiol 2000; 54:735–774
    [Google Scholar]
  36. Straub D, Rothballer M, Hartmann A, Ludewig U. The genome of the endophytic bacterium H. frisingense GSF30(T) identifies diverse strategies in the Herbaspirillum genus to interact with plants. Front Microbiol 2013; 4:168
    [Google Scholar]
  37. Chaves DF, de Souza EM, Monteiro RA. De Oliveira Pedrosa f. a two-dimensional electrophoretic profile of the proteins secreted by Herbaspirillum seropedicae strain Z78. J Proteomics 2009; 73:50–56
    [Google Scholar]
  38. Subsin B, Thomas MS, Katzenmeier G, Shaw JG, Tungpradabkul S et al. Role of the stationary growth phase sigma factor rpoS of Burkholderia pseudomallei in response to physiological stress conditions. J Bacteriol 2003; 185:7008–7014
    [Google Scholar]
  39. Mariappan V, Vellasamy KM, Hashim OH, Vadivelu J. Profiling of Burkholderia cepacia secretome at mid-logarithmic and early-stationary phases of growth. PLoS One 2011; 6:e26518
    [Google Scholar]
  40. Wilson JW, Schurr MJ, LeBlanc CL, Ramamurthy R, Buchanan KL et al. Mechanisms of bacterial pathogenicity. Postgrad Med J 2002; 78:216–224
    [Google Scholar]
  41. Riise GC, Qvarfordt I, Larsson S, Eliasson V, Andersson BA. Inhibitory effect of N-acetylcysteine on adherence of Streptococcus pneumoniae and Haemophilus influenzae to human oropharyngeal epithelial cells in vitro . Respiration 2000; 67:552–558
    [Google Scholar]
  42. Arellano-Reynoso B, Lapaque N, Salcedo S et al. Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 2005; 6:618–625
    [Google Scholar]
  43. Shaver CM, Grove BS, Clune JK, Mackman N, Ware LB et al. Myeloid tissue factor does not modulate lung inflammation or permeability during experimental acute lung injury. Sci Rep 2016; 6:22249
    [Google Scholar]
  44. Heeckeren A, Walenga R, Konstan MW, Bonfield T, Davis PB et al. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J Clin Invest 1997; 100:2810–2815
    [Google Scholar]
  45. Bergeron Y, Ouellet N, Deslauriers AM, Simard M, Olivier M et al. Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect Immun 1998; 66:912–922
    [Google Scholar]
  46. Damjanovic D, Khera A, Medina MF et al. Type 1 interferon gene transfer enhances host defense against pulmonary Streptococcus pneumoniae infection via activating innate leukocytes. Mol Ther Methods Clin Dev 2014; 1:5
    [Google Scholar]
  47. Emery FD, Parvathareddy J, Pandey AK, Cui Y, Williams RW et al. Genetic control of weight loss during pneumonic Burkholderia pseudomallei infection. Pathog Dis 2014; 71:249–264
    [Google Scholar]
  48. Harris G, Kuo Lee R, Lam CK et al. A mouse model of Acinetobacter baumannii-associated pneumonia using a clinically isolated hypervirulent strain. Antimicrob Agents Chemother 2013; 57:3601–3613
    [Google Scholar]
  49. Sordi R, Menezes-de-Lima O, Della-Justina AM, Rezende E, Assreuy J. Pneumonia-induced sepsis in mice: temporal study of inflammatory and cardiovascular parameters. Int J Exp Pathol 2013; 94:144–155
    [Google Scholar]
  50. van Faassen H, KuoLee R, Harris G, Zhao X, Conlan JW et al. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect Immun 2007; 75:5597–5608
    [Google Scholar]
  51. Chen J, Su Z, Liu Y et al. Herbaspirillum species: a potential pathogenic bacteria isolated from acute lymphoblastic leukemia patient. Curr Microbiol 2011; 62:331–333
    [Google Scholar]
  52. Pedrosa FO, Monteiro RA, Wassem R. Et al. genome of Herbaspirillum seropedicae strain SMR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 2011; 7:e1002064
    [Google Scholar]
  53. Fullner KJ, Boucher JC, Hanes MA et al. The contribution of accessory toxins of Vibrio cholerae O1 El Tor to the proinflammatory response in a murine pulmonary cholera model. J Exp Med 2002; 195:1455–1462
    [Google Scholar]
  54. Hawkins P. Recognizing and assessing pain, suffering and distress in laboratory animals: a survey of current practice in the UK with recommendations. Lab Anim 2002; 36:378–395
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001343
Loading
/content/journal/jmm/10.1099/jmm.0.001343
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error