Skip to main navigation menu Skip to main content Skip to site footer
ACI Avances en Ciencias e Ingenierías

SECTION B: LIFE SCIENCES

Vol. 13 No. 1 (2021)

Pseudomonas aeruginosa transition from environmental generalist to human pathogen: Mini-Review

DOI
https://doi.org/10.18272/aci.v13i1.2225
Submitted
March 7, 2021
Published
2021-08-31

Abstract

Opportunistic bacteria Pseudomonas aeruginosa is one of the major concerns as an etiological agent of nosocomial infections in humans. Many virulence factors used to colonize the human body are the same as those used by P. aeruginosa to thrive in the environment such as membrane transport, biofilm formation, oxidation/reduction reaction, among others. P. aeruginosa origin is mainly from the environment, the adaptation to mammalian tissues may follow a source-sink evolution model; the environment is the source of many lineages, some of them capable of adaptation to the human body. Some lineages may adapt to humans and go through reductive evolution in which some genes are lost.  The understanding of this process may be critical to implement better methods to control outbreaks in hospitals.

viewed = 444 times

References

  1. Juan, C., Peña, C., & Oliver, A. (2017). Host and Pathogen Biomarkers for Severe Pseudomonas aeruginosa Infections. The Journal of Infectious Diseases, 215(suppl_1), S44-S51. https://doi.org/10.1093/infdis/jiw299
  2. Ding, C., Yang, Z., Wang, J., Liu, X., Cao, Y., Pan, Y., Han, L., & Zhan, S. (2016). Prevalence of Pseudomonas aeruginosa and antimicrobial-resistant Pseudomonas aeruginosa in patients with pneumonia in mainland China: A systematic review and meta-analysis. International Journal of Infectious Diseases, 49, 119-128. https://doi.org/10.1016/j.ijid.2016.06.014
  3. Ribeiro, Á. C. da S., Crozatti, M. T. L., Silva, A. A. da, Macedo, R. S., Machado, A. M. de O., & Silva, A. T. de A. (2020). Pseudomonas aeruginosa in the ICU: Prevalence, resistance profile, and antimicrobial consumption. Revista da Sociedade Brasileira de Medicina Tropical, 53, e20180498. https://doi.org/10.1590/0037-8682-0498-2018
  4. Monsó, E. (2017). Microbiome in chronic obstructive pulmonary disease. Annals of Translational Medicine, 5(12), 251-251. https://doi.org/10.21037/atm.2017.04.20
  5. Rodrigo-Troyano, A., & Sibila, O. (2017). The respiratory threat posed by multidrug resistant Gram-negative bacteria: MDR-GNB in respiratory infections. Respirology, 22(7), 1288-1299. https://doi.org/10.1111/resp.13115
  6. Teweldemedhin, M., Gebreyesus, H., Atsbaha, A. H., Asgedom, S. W., & Saravanan, M. (2017). Bacterial profile of ocular infections: A systematic review. BMC Ophthalmology, 17(1). https://doi.org/10.1186/s12886-017-0612-2
  7. Roser, D. J., Van Den Akker, B., Boase, S., Haas, C. N., Ashbolt, N. J., & Rice, S. A. (2014). Pseudomonas aeruginosa dose response and bathing water infection. Epidemiology and Infection, 142(03), 449-462. https://doi.org/10.1017/S0950268813002690
  8. Moremi, N., Claus, H., Vogel, U., & Mshana, S. E. (2017). Surveillance of surgical site infections by Pseudomonas aeruginosa and strain characterization in Tanzanian hospitals does not provide proof for a role of hospital water plumbing systems in transmission. Antimicrobial Resistance & Infection Control, 6(1). https://doi.org/10.1186/s13756-017-0216-x
  9. De Soyza, A., & Winstanley, C. (2018). Pseudomonas aeruginosa and Bronchiectasis. En J. Chalmers, E. Polverino, & S. Aliberti (Eds.), Bronchiectasis (pp. 157-180). Springer International Publishing. https://doi.org/10.1007/978-3-319-61452-6_12
  10. Engelhart, S., Krizek, L., Glasmacher, A., Fischnaller, E., Marklein, G., & Exner, M. (2002). Pseudomonas aeruginosa outbreak in a haematology-oncology unit associated with contaminated surface cleaning equipment. Journal of Hospital Infection, 52(2), 93-98. https://doi.org/10.1053/jhin.2002.1279
  11. English, E. L., Schutz, K. C., Willsey, G. G., & Wargo, M. J. (2018). Transcriptional Responses of Pseudomonas aeruginosa to Potable Water and Freshwater. Applied and Environmental Microbiology, 84(6). https://doi.org/10.1128/AEM.02350-17
  12. Hahn, M. W., & Höfle, M. G. (2001). Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiology Ecology, 35(2), 113-121. https://doi.org/10.1111/j.1574-6941.2001.tb00794.x
  13. Abalos, A., Viñas, M., Sabaté, J., Manresa, M. A., & Solanas, A. M. (2004). Enhanced Biodegradation of Casablanca Crude Oil by A Microbial Consortium in Presence of a Rhamnolipid Produced by Pseudomonas aeruginosa AT10. Biodegradation, 15(4), 249-260. https://doi.org/10.1023/B:BIOD.0000042915.28757.fb
  14. Benie, C. K. D., Dadié, A., Guessennd, N., N"™gbesso-Kouadio, N. A., Kouame, N. D., N"™golo, D. C., Aka, S., Dako, E., Dje, K. M., & Dosso, M. (2017). Characterization of virulence potential of Pseudomonas aeruginosa isolated from bovine meat, fresh fish, and smoked fish. European Journal of Microbiology and Immunology, 7(1), 55-64. https://doi.org/10.1556/1886.2016.00039
  15. Das, K., & Mukherjee, A. K. (2007). Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bioresource Technology, 98(7), 1339-1345. https://doi.org/10.1016/j.biortech.2006.05.032
  16. Gupta, B., Kunal, Rajor, A., & Kaur, J. (2018). Isolation, Characterisation of Novel Pseudomonas and Enterobacter sp. From Contaminated Soil of Chandigarh for Naphthalene Degradation. En S. K. Ghosh (Ed.), Utilization and Management of Bioresources (pp. 175-186). Springer Singapore. https://doi.org/10.1007/978-981-10-5349-8_17
  17. Kotresha, D., & Vidyasagar, G. M. (2008). Isolation and characterisation of phenol-degrading Pseudomonas aeruginosa MTCC 4996. World Journal of Microbiology and Biotechnology, 24(4), 541-547. https://doi.org/10.1007/s11274-007-9508-2
  18. Tortell, P. D., Maldonado, M. T., & Price, N. M. (1996). The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature, 383(6598), 330-332. https://doi.org/10.1038/383330a0
  19. Wei, Y.-H., Chou, C.-L., & Chang, J.-S. (2005). Rhamnolipid production by indigenous Pseudomonas aeruginosa J4 originating from petrochemical wastewater. Biochemical Engineering Journal, 27(2), 146-154. https://doi.org/10.1016/j.bej.2005.08.028
  20. Bert, F., Maubec, E., Bruneau, B., Berry, P., & Lambert-Zechovsky, N. (1998). Multi-resistant Pseudomonas aeruginosa outbreak associated with contaminated tap water in a neurosurgery intensive care unit. Journal of Hospital Infection, 39(1), 53-62. https://doi.org/10.1016/S0195-6701(98)90243-2
  21. Meyer, B. (2003). Approaches to prevention, removal and killing of biofilms. International Biodeterioration & Biodegradation, 51(4), 249-253. https://doi.org/10.1016/S0964-8305(03)00047-7
  22. Chatterjee, M., Anju, C., Biswas, L., Anil Kumar, V., Gopi Mohan, C., & Biswas, R. (2016). Antibiotic resistance in Pseudomonas aeruginosa and alternative therapeutic options. International Journal of Medical Microbiology: IJMM, 306(1), 48-58. https://doi.org/10.1016/j.ijmm.2015.11.004
  23. Ruiz-Garbajosa, P., & Cantón, R. (2017). Epidemiology of antibiotic resistance in Pseudomonas aeruginosa. Implications for empiric and definitive therapy. Revista Espanola De Quimioterapia: Publicacion Oficial De La Sociedad Espanola De Quimioterapia, 30 Suppl 1, 8-12.
  24. Subedi, D., Vijay, A. K., & Willcox, M. (2018). Overview of mechanisms of antibiotic resistance in Pseudomonas aeruginosa: An ocular perspective: Mechanism of antimicrobial resistance in P. aeruginosa. Clinical and Experimental Optometry, 101(2), 162-171. https://doi.org/10.1111/cxo.12621
  25. Sokurenko, E. V., Gomulkiewicz, R., & Dykhuizen, D. E. (2006). Source-sink dynamics of virulence evolution. Nature Reviews Microbiology, 4(7), 548-555. https://doi.org/10.1038/nrmicro1446
  26. Dettman, J. R., Rodrigue, N., Aaron, S. D., & Kassen, R. (2013). Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, 110(52), 21065-21070. https://doi.org/10.1073/pnas.1307862110
  27. Dettman, Jeremy R., Rodrigue, N., & Kassen, R. (2015). Genome-Wide Patterns of Recombination in the Opportunistic Human Pathogen Pseudomonas aeruginosa. Genome Biology and Evolution, 7(1), 18-34. https://doi.org/10.1093/gbe/evu260
  28. Pukatzki, S., Kessin, R. H., & Mekalanos, J. J. (2002). The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proceedings of the National Academy of Sciences of the United States of America, 99(5), 3159-3164. https://doi.org/10.1073/pnas.052704399
  29. Wolfgang, M. C., Kulasekara, B. R., Liang, X., Boyd, D., Wu, K., Yang, Q., Miyada, C. G., & Lory, S. (2003). Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, 100(14), 8484-8489. https://doi.org/10.1073/pnas.0832438100
  30. Abd, H., Wretlind, B., Saeed, A., Idsund, E., Hultenby, K., & Sandstrã-M, G. (2008). Pseudomonas aeruginosa Utilises Its Type III Secretion System to Kill the Free-Living Amoeba Acanthamoeba castellanii. Journal of Eukaryotic Microbiology, 55(3), 235-243. https://doi.org/10.1111/j.1550-7408.2008.00311.x
  31. Matz, C., Moreno, A. M., Alhede, M., Manefield, M., Hauser, A. R., Givskov, M., & Kjelleberg, S. (2008). Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae. The ISME Journal, 2(8), 843-852. https://doi.org/10.1038/ismej.2008.47
  32. Hauser, A. R. (2009). The type III secretion system of Pseudomonas aeruginosa: Infection by injection. Nature Reviews Microbiology, 7(9), 654-665. https://doi.org/10.1038/nrmicro2199
  33. Epelman, S., Stack, D., Bell, C., Wong, E., Neely, G. G., Krutzik, S., Miyake, K., Kubes, P., Zbytnuik, L. D., Ma, L. L., Xie, X., Woods, D. E., & Mody, C. H. (2004). Different Domains of Pseudomonas aeruginosa Exoenzyme S Activate Distinct TLRs. The Journal of Immunology, 173(3), 2031-2040. https://doi.org/10.4049/jimmunol.173.3.2031
  34. Teitzel, G. M., Geddie, A., De Long, S. K., Kirisits, M. J., Whiteley, M., & Parsek, M. R. (2006). Survival and Growth in the Presence of Elevated Copper: Transcriptional Profiling of Copper-Stressed Pseudomonas aeruginosa. Journal of Bacteriology, 188(20), 7242-7256. https://doi.org/10.1128/JB.00837-06
  35. Schalk, I. J., & Guillon, L. (2013). Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: Implications for metal homeostasis: Pyoverdine biosynthesis. Environmental Microbiology, 15(6), 1661-1673. https://doi.org/10.1111/1462-2920.12013
  36. Meyer, J. M., Neely, A., Stintzi, A., Georges, C., & Holder, I. A. (1996). Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infection and Immunity, 64(2), 518-523.
  37. Touati, D. (2000). Iron and Oxidative Stress in Bacteria. Archives of Biochemistry and Biophysics, 373(1), 1-6. https://doi.org/10.1006/abbi.1999.1518
  38. Silby, M. W., Winstanley, C., Godfrey, S. A. C., Levy, S. B., & Jackson, R. W. (2011). Pseudomonas genomes: Diverse and adaptable. FEMS Microbiology Reviews, 35(4), 652-680. https://doi.org/10.1111/j.1574-6976.2011.00269.x
  39. Pirnay, J.-P., Bilocq, F., Pot, B., Cornelis, P., Zizi, M., Van Eldere, J., Deschaght, P., Vaneechoutte, M., Jennes, S., Pitt, T., & De Vos, D. (2009). Pseudomonas aeruginosa Population Structure Revisited. PLoS ONE, 4(11), e7740. https://doi.org/10.1371/journal.pone.0007740
  40. Parcell, B. J., Oravcova, K., Pinheiro, M., Holden, M. T. G., Phillips, G., Turton, J. F., & Gillespie, S. H. (2018). Pseudomonas aeruginosa intensive care unit outbreak: Winnowing of transmissions with molecular and genomic typing. Journal of Hospital Infection, 98(3), 282-288. https://doi.org/10.1016/j.jhin.2017.12.005
  41. Quick, J., Cumley, N., Wearn, C. M., Niebel, M., Constantinidou, C., Thomas, C. M., Pallen, M. J., Moiemen, N. S., Bamford, A., Oppenheim, B., & Loman, N. J. (2014). Seeking the source of Pseudomonas aeruginosa infections in a recently opened hospital: An observational study using whole-genome sequencing. BMJ Open, 4(11), e006278. https://doi.org/10.1136/bmjopen-2014-006278
  42. Sánchez, D., Gomila, M., Bennasar, A., Lalucat, J., & García-Valdés, E. (2014). Genome Analysis of Environmental and Clinical Pseudomonas aeruginosa Isolates from Sequence Type-1146. PLoS ONE, 9(10), e107754. https://doi.org/10.1371/journal.pone.0107754
  43. Lucchetti-Miganeh, C., Redelberger, D., Chambonnier, G., Rechenmann, F., Elsen, S., Bordi, C., Jeannot, K., Attrée, I., Plésiat, P., & de Bentzmann, S. (2014). Pseudomonas aeruginosa Genome Evolution in Patients and under the Hospital Environment. Pathogens, 3(2), 309-340. https://doi.org/10.3390/pathogens3020309
  44. Mahenthiralingam, E., Campbell, M. E., & Speert, D. P. (1994). Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infection and Immunity, 62(2), 596-605.
  45. Diaz Caballero, J., Clark, S. T., Coburn, B., Zhang, Y., Wang, P. W., Donaldson, S. L., Tullis, D. E., Yau, Y. C. W., Waters, V. J., Hwang, D. M., & Guttman, D. S. (2015). Selective Sweeps and Parallel Pathoadaptation Drive Pseudomonas aeruginosa Evolution in the Cystic Fibrosis Lung. MBio, 6(5). https://doi.org/10.1128/mBio.00981-15
  46. Tamburini, F. B., Andermann, T. M., Tkachenko, E., Senchyna, F., Banaei, N., & Bhatt, A. S. (2018). Precision identification of diverse bloodstream pathogens in the gut microbiome. Nature Medicine, 24(12), 1809-1814. https://doi.org/10.1038/s41591-018-0202-8
  47. Cholley, P., Thouverez, M., Hocquet, D., van der Mee-Marquet, N., Talon, D., & Bertrand, X. (2011). Most Multidrug-Resistant Pseudomonas aeruginosa Isolates from Hospitals in Eastern France Belong to a Few Clonal Types. Journal of Clinical Microbiology, 49(7), 2578-2583. https://doi.org/10.1128/JCM.00102-11
  48. Bhagirath, A. Y., Li, Y., Somayajula, D., Dadashi, M., Badr, S., & Duan, K. (2016). Cystic fibrosis lung environment and Pseudomonas aeruginosa infection. BMC Pulmonary Medicine, 16(1). https://doi.org/10.1186/s12890-016-0339-5
  49. Williams, B. J., Dehnbostel, J., & Blackwell, T. S. (2010). Pseudomonas aeruginosa: Host defense in lung diseases. Respirology, 15(7), 1037-1056. https://doi.org/10.1111/j.1440-1843.2010.01819.x
  50. Perron, G. G., Gonzalez, A., & Buckling, A. (2007). Source-sink dynamics shape the evolution of antibiotic resistance and its pleiotropic fitness cost. Proceedings of the Royal Society B: Biological Sciences, 274(1623), 2351-2356. https://doi.org/10.1098/rspb.2007.0640
  51. Holt, R. D., Barfield, M., & Gomulkiewicz, R. (2004). Temporal Variation Can Facilitate Niche Evolution in Harsh Sink Environments. The American Naturalist, 164(2), 187-200. https://doi.org/10.1086/422343
  52. Kassen, R. (2002). The experimental evolution of specialists, generalists, and the maintenance of diversity: Experimental evolution in variable environments. Journal of Evolutionary Biology, 15(2), 173-190. https://doi.org/10.1046/j.1420-9101.2002.00377.x
  53. Juárez-Vázquez, A. L., Edirisinghe, J. N., Verduzco-Castro, E. A., Michalska, K., Wu, C., Noda-García, L., Babnigg, G., Endres, M., Medina-Ruíz, S., Santoyo-Flores, J., Carrillo-Tripp, M., Ton-That, H., Joachimiak, A., Henry, C. S., & Barona-Gómez, F. (2017). Evolution of substrate specificity in a retained enzyme driven by gene loss. ELife, 6. https://doi.org/10.7554/eLife.22679
  54. Zhang, X., Liu, X., Liang, Y., Guo, X., Xiao, Y., Ma, L., Miao, B., Liu, H., Peng, D., Huang, W., Zhang, Y., & Yin, H. (2017). Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss. Applied and Environmental Microbiology, 83(7). https://doi.org/10.1128/AEM.03098-16
  55. Moran, N. A. (2002). Microbial minimalism: Genome reduction in bacterial pathogens. Cell, 108(5), 583-586.
  56. Andersen, S. B., Ghoul, M., Griffin, A. S., Petersen, B., Johansen, H. K., & Molin, S. (2017). Diversity, Prevalence, and Longitudinal Occurrence of Type II Toxin-Antitoxin Systems of Pseudomonas aeruginosa Infecting Cystic Fibrosis Lungs. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.01180
  57. Barth, A. L., & Pitt, T. L. (1996). The high amino-acid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa. Journal of Medical Microbiology, 45(2), 110-119. https://doi.org/10.1099/00222615-45-2-110
  58. Thomas, S. R. (2000). Increased sputum amino acid concentrations and auxotrophy of Pseudomonas aeruginosa in severe cystic fibrosis lung disease. Thorax, 55(9), 795-797. https://doi.org/10.1136/thorax.55.9.795
  59. Huse, H. K., Kwon, T., Zlosnik, J. E. A., Speert, D. P., Marcotte, E. M., & Whiteley, M. (2010). Parallel Evolution in Pseudomonas aeruginosa over 39,000 Generations In Vivo. MBio, 1(4). https://doi.org/10.1128/mBio.00199-10
  60. Nguyen, A. T., O"™Neill, M. J., Watts, A. M., Robson, C. L., Lamont, I. L., Wilks, A., & Oglesby-Sherrouse, A. G. (2014). Adaptation of Iron Homeostasis Pathways by a Pseudomonas aeruginosa Pyoverdine Mutant in the Cystic Fibrosis Lung. Journal of Bacteriology, 196(12), 2265-2276. https://doi.org/10.1128/JB.01491-14
  61. Ghio, A. J., Roggli, V. L., Soukup, J. M., Richards, J. H., Randell, S. H., & Muhlebach, M. S. (2013). Iron accumulates in the lavage and explanted lungs of cystic fibrosis patients. Journal of Cystic Fibrosis, 12(4), 390-398. https://doi.org/10.1016/j.jcf.2012.10.010
  62. Wegiel, B., Nemeth, Z., Correa-Costa, M., Bulmer, A. C., & Otterbein, L. E. (2014). Heme Oxygenase-1: A Metabolic Nike. Antioxidants & Redox Signaling, 20(11), 1709-1722. https://doi.org/10.1089/ars.2013.5667
  63. Huse, H. K., Kwon, T., Zlosnik, J. E. A., Speert, D. P., Marcotte, E. M., & Whiteley, M. (2013). Pseudomonas aeruginosa Enhances Production of a Non-Alginate Exopolysaccharide during Long-Term Colonization of the Cystic Fibrosis Lung. PLoS ONE, 8(12), e82621. https://doi.org/10.1371/journal.pone.0082621
  64. Smith, E. E., Buckley, D. G., Wu, Z., Saenphimmachak, C., Hoffman, L. R., D"™Argenio, D. A., Miller, S. I., Ramsey, B. W., Speert, D. P., Moskowitz, S. M., Burns, J. L., Kaul, R., & Olson, M. V. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proceedings of the National Academy of Sciences, 103(22), 8487-8492. https://doi.org/10.1073/pnas.0602138103
  65. Oliver, A., Cantón, R., Campo, P., Baquero, F., & Blázquez, J. (2000). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science (New York, N.Y.), 288(5469), 1251-1254
  66. Mena, A., Smith, E. E., Burns, J. L., Speert, D. P., Moskowitz, S. M., Perez, J. L., & Oliver, A. (2008). Genetic Adaptation of Pseudomonas aeruginosa to the Airways of Cystic Fibrosis Patients Is Catalyzed by Hypermutation. Journal of Bacteriology, 190(24), 7910-7917. https://doi.org/10.1128/JB.01147-08
  67. Lam, J., Chan, R., Lam, K., & Costerton, J. W. (1980). Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infection and Immunity, 28(2), 546-556.
  68. Sriramulu, D. D. (2005). Microcolony formation: A novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. Journal of Medical Microbiology, 54(7), 667-676. https://doi.org/10.1099/jmm.0.45969-0
  69. Treepong, P., Kos, V. N., Guyeux, C., Blanc, D. S., Bertrand, X., Valot, B., & Hocquet, D. (2018). Global emergence of the widespread Pseudomonas aeruginosa ST235 clone. Clinical Microbiology and Infection, 24(3), 258-266. https://doi.org/10.1016/j.cmi.2017.06.018
  70. Yang, L., Jelsbak, L., Marvig, R. L., Damkiaer, S., Workman, C. T., Rau, M. H., Hansen, S. K., Folkesson, A., Johansen, H. K., Ciofu, O., Hoiby, N., Sommer, M. O. A., & Molin, S. (2011). Evolutionary dynamics of bacteria in a human host environment. Proceedings of the National Academy of Sciences, 108(18), 7481-7486. https://doi.org/10.1073/pnas.1018249108
  71. Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7(12), 1225-1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
  72. Chatterjee, P., Davis, E., Yu, F., James, S., Wildschutte, J. H., Wiegmann, D. D., Sherman, D. H., McKay, R. M., LiPuma, J. J., & Wildschutte, H. (2017). Environmental Pseudomonads Inhibit Cystic Fibrosis Patient-Derived Pseudomonas aeruginosa. Applied and Environmental Microbiology, 83(2). https://doi.org/10.1128/AEM.02701-16

Most read articles by the same author(s)