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Label-Free Proteomics of a Defined, Binary Co-culture Reveals Diversity of Competitive Responses Between Members of a Model Soil Microbial System

  • Environmental Microbiology
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Abstract

Interactions among members of microbial consortia drive the complex dynamics in soil, gut, and biotechnology microbiomes. Proteomic analysis of defined co-cultures of well-characterized species provides valuable information about microbial interactions. We used a label-free approach to quantify the responses to co-culture of two model bacterial species relevant to soil and rhizosphere ecology, Bacillus atrophaeus and Pseudomonas putida. Experiments determined the ratio of species in co-culture that would result in the greatest number of high-confidence protein identifications for both species. The 281 and 256 proteins with significant shifts in abundance for B. atrophaeus and P. putida, respectively, indicated responses to co-culture in overall metabolism, cell motility, and response to antagonistic compounds. Proteins associated with a virulent phenotype during surface-associated growth were significantly more abundant for P. putida in co-culture. Co-culture on agar plates triggered a filamentous phenotype in P. putida and avoidance of P. putida by B. atrophaeus colonies, corroborating antagonistic interactions between these species. Additional experiments showing increased relative abundance of P. putida under conditions of iron or zinc limitation and increased relative abundance of B. atrophaeus under magnesium limitation were consistent with patterns of changes in abundance of metal-binding proteins during co-culture. These results provide details on the nature of interactions between two species with antagonistic capabilities. Significant challenges remaining for the development of proteomics as a tool in microbial ecology include accurate quantification of low-abundance peptides, especially from rare species present at low relative abundance in a consortium.

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References

  1. Widder S, Allen RJ, Pfeiffer T, et al. (2016) Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J 10:2557–2568. https://doi.org/10.1038/ismej.2016.45

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lopez-Mondejar R, Zuhlke D, Becher D, Riedel K, Baldrian P (2016) Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep 6:25279. https://doi.org/10.1038/srep25279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Prosser JI, Bohannan BJM, Curtis TP, et al. (2007) The role of ecological theory in microbial ecology. Nat Rev Microbiol 5:384–392

    Article  CAS  PubMed  Google Scholar 

  4. Rooks MG, Garrett WS (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16:341–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lloyd-Price J, Abu-Ali G, Huttenhower C (2016) The healthy human microbiome. Genome Med 8:51. https://doi.org/10.1186/s13073-016-0307-y

    Article  PubMed  PubMed Central  Google Scholar 

  6. Jiang Y, Xiong X, Danska J, Parkinson J (2016) Metatranscriptomic analysis of diverse microbial communities reveals core metabolic pathways and microbiome-specific functionality. Microbiome 4:2. https://doi.org/10.1186/s40168-015-0146-x

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lindemann SR, Bernstein HC, Song H-S, Fredrickson JK, Fields MW, Shou W, Johnson DR, Beliaev AS (2016) Engineering microbial consortia for controllable outputs. ISME J 10:2077–2084. https://doi.org/10.1038/ismej.2016.26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Dolinsek J, Goldschmidt F, Johnson DR (2016) Synthetic microbial ecology and the dynamic interplay between microbial genotypes. FEMS Microbiol Rev 40:961–979. https://doi.org/10.1093/femsre/fuw024

    Article  CAS  PubMed  Google Scholar 

  9. Zhang H, Wang X (2016) Modular co-culture engineering, a new approach for metabolic engineering. Metab Eng 37:114–121. https://doi.org/10.1016/j.ymben.2016.05.007

    Article  PubMed  Google Scholar 

  10. Rundell EA, Banta LM, Ward DV, Watts CD, Birren B, Esteban DJ (2014) 16SrRNA gene survey of microbial communities in Winogradsky columns. PLoS One 9:e104134. https://doi.org/10.1371/journal.pone.0104134

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the Illumina platform. PLoS One 10:e0116955. https://doi.org/10.1371/journal.pone.0116955

    Article  PubMed  PubMed Central  Google Scholar 

  12. Langille MGI, Zaneveld J, Caporaso JG, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wallace RJ, Snelling TJ, McCartney CA, Tapio I, Strozzi F (2017) Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism. Genet Sel Evol 49:9. https://doi.org/10.1186/s12711-017-0285-6

    Article  PubMed  PubMed Central  Google Scholar 

  14. Franzosa EA, Hsu T, Sirota-Madi A, Shafquat A, Abu-Ali G, Morgan XC, Huttenhower C (2015) Sequencing and beyond: integrating molecular ‘omics’ for microbial community profiling. Nat Rev Microbiol 13:360–372. https://doi.org/10.1038/nrmicro3451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Baldrian P, Lopez-Mondejar R (2014) Microbial genomics, transcriptomics and proteomics: new discoveries in decomposition research using complementary methods. Appl Microbiol Biotechnol 98:1531–1537

    Article  CAS  PubMed  Google Scholar 

  16. Edfors F, Danielsson F, Hallstrom BM, Kall L, Lundberg E, Ponten F, Forsstrom B, Uhlen M (2016) Gene-specific correlation of RNA and protein levels in human cells and tissues. Mol Syst Biol 12:883. 10.15252/msb.20167144

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wang J, Ma Z, Carr SA, et al. (2017) Proteome profiling outperforms transcriptome profiling for coexpression based gene function prediction. Mol Cell Proteomics 16:121–134

    Article  CAS  PubMed  Google Scholar 

  18. Herbst F-A, Lunsmann V, Kjeldal H, Jehmlich N, Tholey A, von Bergen M, Nielsen JL, Hettich RL, Seifert J, Nielsen PH (2016) Enhancing metaproteomics-the value of models and defined environmental microbial systems. Proteomics 16:783–798. https://doi.org/10.1002/pmic.201500305

    Article  CAS  PubMed  Google Scholar 

  19. Giannone RJ, Huber H, Karpinets T, Heimerl T, Kuper U, Rachel R, Keller M, Hettich RL, Podar M (2011) Proteomic characterization of cellular and molecular processes that enable the Nanoarchaeum equitans-Ignicoccus hospitalis relationship. PLoS One 6:e22942. https://doi.org/10.1371/journal.pone.0022942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Muddiman D, Andrews G, Lewis D, Notey J, Kelly R (2010) Part II: defining and quantifying individual and co-cultured intracellular proteomes of two thermophilic microorganisms by GeLC-MS2 and spectral counting. Anal Bioanal Chem 398:391–404. https://doi.org/10.1007/s00216-010-3929-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ruiz L, Sanchez B, de los Reyes-Gavilan CG, Gueimonde M, Margolles A (2009) Coculture of Bifidobacterium longum and Bifidobacterium breve alters their protein expression profiles and enzymatic activities. Int J Food Microbiol 133:148–153

    Article  CAS  PubMed  Google Scholar 

  22. Di Cagno R, De Angelis M, Coda R, Minervini F, Gobbetti M (2009) Molecular adaptation of sourdough Lactobacillus plantarum DC400 under co-cultivation with other lactobacilli. Res Microbiol 160:358–366

    Article  PubMed  Google Scholar 

  23. Sedlacek CJ, Nielsen S, Greis KD, Haffey WD, Revsbech NP, Ticak T, Laanbroek HJ, Bollmann A (2016) Effects of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. strain Is79. Appl Environ Microbiol 82:4776–4788. https://doi.org/10.1128/AEM.01171-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sieber JR, Crable BR, Sheik CS, Hurst GB, Rohlin L, Gunsalus RP, McInerney MJ (2015) Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei. Front Microbiol 6:115. https://doi.org/10.3389/fmicb.2015.00115

    Article  PubMed  PubMed Central  Google Scholar 

  25. Klein MI, Xiao J, Lu B, Delahunty CM, Yates III JR, et al. (2012) Streptococcus mutans protein synthesis during mixed-species biofilm development by high-throughput quantitative proteomics. PLoS One 7:e45795. https://doi.org/10.1371/journal.pone.0045795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kluge S, Hoffman M, Benndorf D, Rapp E, Reichl U (2012) Proteomic tracking and analysis of a bacterial mixed culture. Proteomics 12:1893–1901. https://doi.org/10.1002/pmic.201100362

    Article  CAS  PubMed  Google Scholar 

  27. Huang EL, Lefsrud MG (2012) Temporal analysis of xylose fermentation by Scheffersomyces stipites using shotgun proteomics. J Ind Microbiol Biotechnol 39:1507–1514

    Article  CAS  PubMed  Google Scholar 

  28. Enoki M, Shinzato N, Sato H, Nakamura K, Kamagata Y (2011) Comparative proteomic analysis of Methanothermobacter themautotrophicus ΔH in pure culture and in co-culture with a butyrate-oxidizing bacterium. PLoS One 6:e24309. https://doi.org/10.1371/journal.pone.0024309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Men Y, Feil H, VerBerkmoes NC, Shah MB, Johnson DR, Lee PKH, West KA, Zinder SH, Anderson GL, Alvarez-Cohen L (2012) Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomics analysis. ISME J 6:410–421

    Article  CAS  PubMed  Google Scholar 

  30. Ma Q, Zhou J, Zhang W, Meng X, Sun J, et al. (2011) Integrated proteomic and Metabolomic analysis of an artificial microbial Community for two-Step Production of vitamin C. PLoS One 6:e26108. https://doi.org/10.1371/journal.pone.0026108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kouzuma A, Kaku N, Watanabe K (2014) Microbial electricity generation in rice paddy fields: recent advances and perspectives in rhizosphere microbial fuel cells. Appl Microbiol Biotechnol 98:9521. https://doi.org/10.1007/s00253-014-6138-0

    Article  CAS  PubMed  Google Scholar 

  32. Bakker MG, Schlatter DC, Otto-Hanson L, Kinkel LL (2013) Diffuse symbioses: roles of plant-plant, plant-microbe and microbe-microbe interactions in structuring the soil microbiome. Mol Ecol 23:1571–1583

    Article  PubMed  Google Scholar 

  33. Ren D, Madsen JS, Sorensen SJ, Burmolle M (2015) High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J 9:81–89. https://doi.org/10.1038/ismej.2014.96

    Article  CAS  PubMed  Google Scholar 

  34. Kent AD, Triplett EW (2002) Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu Rev Microbiol 56:211–236

    Article  CAS  PubMed  Google Scholar 

  35. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept and review. Soil Biol Biochem 83:184–199

    Article  CAS  Google Scholar 

  36. Tyc O, van den Berg M, Gerards S, van Veen JA, Raaijmakers JM, de Boer W, Garbeva P (2014) Impact of interspecific interactions on antimicrobial activity among soil bacteria. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00567

  37. Liu B, Liu J, Ju M, Li X, Yu Q (2016) Purification and characterization of biosurfactant produced by Bacillus licheniformis Y-1 and its application in remediation of petroleum contaminated soil. Mar Pollut Bull 107:46–51

  38. Barlow J, Gozzi K, Kelley CP, Geilich BM, Webster TJ, Chai Y, Sridhar S, van de Ven AL (2017) High throughput microencapsulation of Bacillus subtilis in semi-permeable biodegradable polymersomes for selenium remediation. Appl Microbiol Biotechnol 101:455–464

    Article  CAS  PubMed  Google Scholar 

  39. Rani A, Souche Y, Goel R (2012) Comparative in situ remediation potential of Pseudomonas putida 710A and Commamonas aquatica 710B using plant (Vigna radiate (L.) wilczek) assay. Ann Microbiol 63:923–928

    Article  Google Scholar 

  40. Gasc C, Richard J-Y, Peyret P (2016) Genome sequence of Pseudomonassp. HUK17, isolated from hexachlorocyclohexane-contaminated soil. Genome Announc 4:e00275–e00216. https://doi.org/10.1128/genomeA.00275-16

    PubMed  PubMed Central  Google Scholar 

  41. Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J-h (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15:848–864

    Article  PubMed  Google Scholar 

  42. Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS One 7:e35498. https://doi.org/10.1371/journal.pone.0035498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Abo-Aba SEM, Sabir JSM, Baeshen MN, Sabir MJ, Mutwakil MHZ, Baeshen NA, D’Amore R, Hall N (2015) Draft genome sequence of Bacillus species from the rhizosphere of the desert plant Rhazya stricta. Genome Announc 3:e00957–e00915. https://doi.org/10.1128/genomeA.00957-15

    Article  PubMed  PubMed Central  Google Scholar 

  44. Simoes M, Simoes LC, Pereira MO, Vieira MJ (2008) Antagonism between Bacillus cereus and Pseudomonas fluorescens in planktonic systems and in biofilms. Biofouling 24:339–349

    Article  CAS  PubMed  Google Scholar 

  45. Mukherjee AK, Bordoloi NK (2012) Biodegradation of benzene, toluene, and xylene (BTX) in liquid culture and in soil by Bacillus subtilis and Pseudomonas aeruginosa strains and a formulated bacterial consortium. Environ Sci Pollut Res 19:3380–3388

    Article  CAS  Google Scholar 

  46. Jousset A, Bienhold C, Chatzinotas A, et al. (2017) Where less may be more: how the rare biosphere pulls ecosystem strings. ISME J 11:853–862

    Article  PubMed  PubMed Central  Google Scholar 

  47. Hausmann B, Knorr K-H, Schreck K, Tringe SG, del Rio TG, Loy A, Pester M (2016) Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms. ISME J. https://doi.org/10.1038/ismej.2016.42

  48. Mallet CR, Lu Z, Mazzeo JR (2004) A study of ion suppression effects in electrospray ionization from mobile phase additives and solid-phase extracts. Rapid Commun Mass Spectrom 18:49–58. https://doi.org/10.1002/rcm.1276

    Article  CAS  PubMed  Google Scholar 

  49. Choi H, Nesvizhskii AI (2008) False discovery rates and related statistical concepts in mass spectrometry-based proteomics. J Proteome Res 7:47–50. https://doi.org/10.1021/pr700747q

    Article  CAS  PubMed  Google Scholar 

  50. Domon B, Aebersold R (2010) Options and considerations when selecting a quantitative protoemics strategy. Nat Biotechnol 28:710–721. https://doi.org/10.1038/nbt.1661

    Article  CAS  PubMed  Google Scholar 

  51. Hageman JH, Shankweiler GW, Wall PR, Franich K, McCowan GW, Cauble SM, Grajeda J, Quinones C (1984) Single, chemically defined sporulation medium for Bacillus subtilis: growth, sporulation and extracellular protease production. J Bacteriol 160:438–441

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Roxas BAP, Li Q (2008) Significance analysis of microarray for relative quantitation of LC/MS data in proteomics. BMC Bioinformatics 9:187. https://doi.org/10.1186/1471-2105-9-187

    Article  PubMed  PubMed Central  Google Scholar 

  53. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B Stat Methodol 64:479–498. https://doi.org/10.1111/1467-9868.00346

    Article  Google Scholar 

  54. Ackermann BL, Berna MJ (2007) Coupling immunoaffinity techniques with MS for quantitative analysis of low-abundance protein biomarkers. Expert Rev Proteomics 4:175–186. https://doi.org/10.1586/14789450.4.2.175

    Article  CAS  PubMed  Google Scholar 

  55. Schalk IJ, Guillon L (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15:1661–1673. https://doi.org/10.1111/1462-2920.12013

    Article  CAS  PubMed  Google Scholar 

  56. de Oliveira ML, Andrade AFB, Vale MD, et al. (2003) Effects of iron limitation on adherence and cell surface carbohydrates of Corynebacterium diphtheria strains. Appl Environ Microbiol 69:5907–5913. https://doi.org/10.1128/AEM.69.10.5907-5913.2003

    Article  Google Scholar 

  57. Blair JMA, Richmond GE, Piddock LJV (2014) Multidrug efflux pumps in Gram-negative bacteria and their role in antibiotic resistance. Future Microbiol 9:1165–1177. https://doi.org/10.2217/fmb.14.66

    Article  CAS  PubMed  Google Scholar 

  58. Overhage J, Bains M, Brazas MD, Hancock REW (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190:2671–2679. https://doi.org/10.1128/JB.01659-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lehnik-Habrink M, Lewis RJ, Mader U, Stulke J (2012) RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. Mol Microbiol 84:1005–1017. https://doi.org/10.1111/j.1365-2958.2012.08072.x

    Article  CAS  PubMed  Google Scholar 

  60. Loose M, Mitchison TJ (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16:38–46. https://doi.org/10.1038/ncb2885

    Article  CAS  PubMed  Google Scholar 

  61. Shih Y-L, Rothfield L (2006) The bacterial cytoskeleton. Microbiol Mol Rev 70:729–754. https://doi.org/10.1128/MMBR.00017-06

    Article  CAS  Google Scholar 

  62. Busuioc M, Mackiewicz K, Buttaro BA, Piggot PJ (2009) Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol 191:7315–7322. https://doi.org/10.1128/JB.00425-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Grossman TH, Tuckman M, Ellestad S, Osbourne MS (1993) Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes. J Bacteriol 175:6203–6211. https://doi.org/10.1128/jb.175.19.6203-6211.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Schneider R, Hantke K (1993) Iron-hydroxamate uptake systems in Bacillus subtilis: identification of a lipoprotein as part of a binding protein-dependent transport system. Mol Microbiol 8:111–121. https://doi.org/10.1111/j.1365-2958.1993.tb01208.x

    Article  CAS  PubMed  Google Scholar 

  65. Keshishian H, Addona T, Burgess M, Kuhn E, Carr SA (2007) Abundance proteins in plasma by targeted mass spectrometry and stabile isotope dilution. Mol Cell Proteomics 6:2212–2229. https://doi.org/10.1074/mcp.M700354-MCP200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yao S, Richards J, Belasco JG, Bechhofer DH (2011) Decay of a model mRNA in Bacillus subtilis by a combination of RNase J1 5′ exonuclease and RNase Y endonuclease activities. J Bacteriol 193:6384–6386. https://doi.org/10.1128/JB.05939-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Leifert C, Li H, Chidburee S, Hampson S, Workman S, Sigee D, Epton HAS, Harbour A (1995) Antibiotic production and biocontrol activity by Bacillus subtilis CL27 and Bacillus pumilis CL45. J Appl Microbiol 78:97–108. https://doi.org/10.1111/j.1365-2672.1995.tb02829.x

    CAS  Google Scholar 

  68. Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256. https://doi.org/10.1094/PHYTO-97-2-0250

    Article  PubMed  Google Scholar 

  69. Kim Y, Cho J-Y, Kuk J-H, Moon J-H, Cho J-I, Kim Y-C, Park K-H (2004) Identification and antimicrobial activity of phenylacetic acid produced by Bacillus licheniformis isolated from fermented soybean, Chungkook-Jang. Curr Microbiol 48:312–317. https://doi.org/10.1007/s00284-003-4193-3

    Article  CAS  PubMed  Google Scholar 

  70. Chun J, Bae KS (2000) Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie Van Leeuwenhoek 78:123–127. https://doi.org/10.1023/A:1026555830014

    Article  CAS  PubMed  Google Scholar 

  71. Parsons JF, Song F, Parsons L, Calabrese K, Eisenstein E, Ladner JE (2004) Structure and function of the phenazine biosynthesis protein PhzF from Pseudomonas fluorescens 2-79. Biochemistry 43:12427–12435. https://doi.org/10.1021/bi049059z

    Article  CAS  PubMed  Google Scholar 

  72. Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445. https://doi.org/10.1146/annurev.phyto.44.013106.145710

    Article  CAS  PubMed  Google Scholar 

  73. Wood DW, Piersen LS (1996) The phzI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168:49–53. https://doi.org/10.1016/0378-1119(95)00754-7

    Article  CAS  PubMed  Google Scholar 

  74. Piersen LS, Piersen EA (1996) Phenazine antibiotic production in Pseudomonas aureofaciens: role in rhizosphere ecology and pathogen suppression. FEMS Microbiol Lett 136:101–108. https://doi.org/10.1016/0378-1097(95)00489-0

    Article  Google Scholar 

  75. Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking ‘secondary’ metabolism:physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78. https://doi.org/10.1038/nchembio764

    Article  CAS  PubMed  Google Scholar 

  76. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193:3606–3617. https://doi.org/10.1128/JB.00396-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Toohey JI, Nelson CD, Krotkov G (1965) Isolation and identification of two phenazines from a strain of Pseudomonas aureofaciens. Can J Bot 43:1055–1062. https://doi.org/10.1139/b65-122

    Article  CAS  Google Scholar 

  78. Caiazza NC, Shanks RMQ, O’Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187:7351–7361. https://doi.org/10.1128/JB.187.21.7351-7361.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Li K, Xu C, Jin Y, Sun Z, Liu C, Shi J, Chen G, Chen R, Jin S, Wu W (2013) SuhB is a regulator of multiple virulence genes and essential for pathogenesis of Pseudomonas aeruginosa. MBio 4:e00419–e00413. https://doi.org/10.1128/mBio.00419-13

    PubMed  PubMed Central  Google Scholar 

  80. Sakhtah H, Koyama L, Zhang Y, Morales DK, Fields BL, Price-Whelan A, Hogan DA, Shepard K, Dietrich LEP (2016) The Pseduomonas aeruginosa efflux pump MexGHI-OpmD transports a natural phenazine that controls gene expression and biofilm development. Proc Natl Acad Sci 113:3538–3547. https://doi.org/10.1073/pnas.1600424113

    Article  Google Scholar 

  81. Das T, Kutty SK, Tavallaie R, Ibugo AI, Panchompoo J, Sehar S, Aldous L, Yeung AWS, Thomas SR, Kumar N, Gooding JJ, Manefield M (2015) Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation. Sci Rep 5. https://doi.org/10.1038/srep08398

  82. Ghadaksaz A, Fooladi AAI, Hosseini HM, Amin M (2015) The prevalence of some Pseudomonas virulence genes related to biofilm formation and alginate production among clinical isolates. J Appl Biomed 13:61–68. https://doi.org/10.1016/j.jab.2014.05.002

    Article  Google Scholar 

  83. Bardoel BW, van der Ent S, Pel MJC, Tommassen J, Pieterse CMJ, van Kessel KPM, et al. (2011) Pseudomonas evades immune recognition of Flagellin in both mammals and plants. PLoS Pathog 7:e1002206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Boyd A, Chakrabarty AM (1995) Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide 15:162–168. https://doi.org/10.1007/BF01569821

  85. Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M, Parsek MR (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183:5395–5401. https://doi.org/10.1128/JB.183.18.5395-5401.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Osman KM, Amer AM, Badr JM, Helmy NM, Elhelw RA, Orabi A, Bakry M, Saad ASA (2016) Antimicrobial resistance, biofilm formation and mecA characterization of methicillin-susceptible S. aureus and non-S.aureus of beef meat origin in Egypt. Front Microbiol 7:222. https://doi.org/10.3389/fmicb.2016.00222

    PubMed  PubMed Central  Google Scholar 

  87. Redgrave LS, Sutton SB, Webber MA, Piddock LJV (2014) Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22:438–445. https://doi.org/10.1016/j.tim.2014.04.007

    Article  CAS  PubMed  Google Scholar 

  88. Tamura M, Lee K, Miller CA, Moore CJ, Shirako Y, Kobayashi M, Cohen SN (2006) RNase E maintenance of proper FtsZ/FtsA ratio required for nonfilamentous growth of Escherichia coli cells but not for colony-forming ability. J Bacteriol 188:5145–5152. https://doi.org/10.1128/JB.00367-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Lutkenhaus J (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the z ring. Annu Rev Biochem 76:539–562. https://doi.org/10.1146/annurev.biochem.75.103004.142652

    Article  CAS  PubMed  Google Scholar 

  90. Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8:634–644. https://doi.org/10.1038/nrmicro2405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kohler T, Curty LK, Barja F, van Delden C, Pechere J-C (2000) Swarming of Pseduomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990–5996. https://doi.org/10.1128/JB.182.21.5990-5996.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Stubbendieck RM, Straight PD (2016) Escape from lethal bacterial competition through coupled activation of antibiotic resistance and a mobilized subpopulation. PLoS Genet 12:e1005807. https://doi.org/10.1371/journal.pgen.1005722

    Article  PubMed  PubMed Central  Google Scholar 

  93. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86:628–644. https://doi.org/10.1111/mmi.12008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Mulcahy H, Lewenza S (2011) Magnesium limitation is an environmental trigger of the Pseudomonas aeruginosa biofilm lifestyle. PLoS One 6:e23307. https://doi.org/10.1371/journal.pone.0023307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. https://doi.org/10.1038/nrmicro2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Hotta K, Kim C-Y, Fox DT, Koppisch AT (2010) Siderophore-mediated iron acquisition in Bacillus anthracis and related strains. Microbiology 156:1918–1925. https://doi.org/10.1099/mic.0.039404-0

    Article  CAS  PubMed  Google Scholar 

  97. Schalk IJ (2008) Metal trafficking via siderophores in Gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J Inorg Biochem 102:1159–1169. https://doi.org/10.1016/j.jinorgbio.2007.11.017

    Article  CAS  PubMed  Google Scholar 

  98. Joshi H, Dave R, Venugopalan VP (2014) Pumping iron to keep fit: modulation of siderophore secretion helps efficient aromatic utilization in Pseudomonas putida KT2440. Microbiology 160:1393–1400. https://doi.org/10.1099/mic.0.079277-0

    Article  CAS  PubMed  Google Scholar 

  99. Prestel E, Noirot P, Auger S (2015) Genome-wide identification of Bacillus subtilis Zur-binding sites associated with a Zur box expands its known regulatory network. BMC Microbiol 15:13. https://doi.org/10.1186/s12866-015-0345-4

    Article  PubMed  PubMed Central  Google Scholar 

  100. D’Orazio M, Mastropasqua MC, Cerasi M, Pacello F, Conosalvo A, Chirullo B, Mortensen B, Skaar EP, Ciavardelli D, Pasquali P, Battistoni A (2015) The capability of Pseudomonas aeruginosa to recruit zinc under conditions of limited metal availability is affected by inactivation of the ZnuABC transporter. Metallomics 7:1023–1035. https://doi.org/10.1039/C5MT00017C

    Article  PubMed  PubMed Central  Google Scholar 

  101. Gielda LM, DiRita VJ (2012) Zinc competition among the intestinal microbiota. MBio 3:00171–00112. https://doi.org/10.1128/mBio.00171-12

    Article  Google Scholar 

  102. Joo J-H, Hassan SHA, Oh S-E (2010) Comparative study of biosorption of Zn2+ by Pseudomonas aeruginosa and Bacillus cereus. Int Biodeterior Biodegrad 64:734–741. https://doi.org/10.1016/j.ibiod.2010.08.007

    Article  CAS  Google Scholar 

  103. Andersen GG, Yahr TL, Lovewell RR, O’Toole GA (2010) The Pseudomonas aeruginosa magnesium transporter MgtE inhibits transcription of the type III secretion system. Infect Immun 78:1239–1249. https://doi.org/10.1128/IAI.00865-09

    Article  Google Scholar 

  104. Song B, Leff LG (2006) Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol Res 161:355–361. https://doi.org/10.1016/j.micres.2006.01.004

    Article  CAS  PubMed  Google Scholar 

  105. Guina T, Wu M, Miller SI, Purvine SO, Yi EC, Eng J, Goodlett DR, Aebersold R, Ernst RK, Lee KA (2003) Proteomic analysis of Pseudomonas aeruginosa grown under magnesium limitation. J Am Soc Mass Spectrom 14:742–751. https://doi.org/10.1016/S1044-0305(03)00133-8

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grants from the Colorado Center for Biorefining and Bioproducts and the Jud and Pat Harper Endowment in the Department of Chemical and Biological Engineering at Colorado State University.

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Chignell, J.F., Park, S., Lacerda, C.M.R. et al. Label-Free Proteomics of a Defined, Binary Co-culture Reveals Diversity of Competitive Responses Between Members of a Model Soil Microbial System. Microb Ecol 75, 701–719 (2018). https://doi.org/10.1007/s00248-017-1072-1

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