Advertisement

Environmental proteomic studies: closer step to understand bacterial biofilms

  • Anupama Rani
  • Subramanian Babu
Review

Abstract

Advancement in proteome analytical techniques and the development of protein databases have been helping to understand the physiology and subtle molecular mechanisms behind biofilm formation in bacteria. This review is to highlight how the evolving proteomic approaches have revealed fundamental molecular processes underlying the formation and regulation of bacterial biofilms. Based on the survey of research reports available on differential expression of proteins in biofilms of bacterial from wide range of environments, four important cellular processes viz. metabolism, motility, transport and stress response that contribute to formation of bacterial biofilms are discussed. This review might answer how proteins related to these cellular processes contribute significantly in stabilizing biofilms of different bacteria in diverse environmental conditions.

Graphical Abstract

Keywords

Bacteria Biofilm Proteomics Tools Techniques 

Abbreviations

DNA

Deoxyribonucleic acid

SDS-PAGE

Sodium dodecyl sulphate polyacrylamide gel electrophoresis

2-DE

Two dimensional polyacrylamide gel electrophoresis

MS

Mass spectrometry

ICAT

Isotope coded affinity tag

iTRAC

Isobaric tag for relative and absolute quantitation

TMTs

Tandem mass tags

AMD

Acid mine drainage

3D, OD

Optical densitometry

DIGE

Difference gel electrophoresis

MALDI-ToF-MS

Matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry

ESI-Q-IT-MS

Electrospray ionization-quadrupole ion trap mass spectrometry

nanoLC-MS/MS

Nano liquid chromatography-mass spectrometry

LC-ESI, TCA

Tricarboxylic acid cycle

c-di-GMP

Bis-(3′-5′)-cyclic dimeric guanosine monophosphate

RNA

Ribonucleic acids

ABC

ATP-binding cassette

ATP

Adenosine triphosphate

TRAP

Tripartite ATP-independent periplasmic

ROS

Reactive oxygen species

OMVs

Outer membrane vesicles

Notes

Acknowledgements

The authors gratefully acknowledge the support rendered by the management of Vellore Institute of Technology, Vellore, India in carrying out their research.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interests.

Research involving human participants and/or animals

The research work does not involve human participants and/or animals.

Informed consent

The research work does not involve human participants and hence informed consent does not arise.

References

  1. Abidin ZZ, Veith PD, Dashper SG, Zhu Y, Catmull DV, Chen YY, Heryanto DC, Chen D, Pyke JS, Tan K, Mitchell HL, Peynolds EC (2012) Differential proteomic analysis of a polymicrobial biofilm. J Proteome Res 11:4449–4464CrossRefGoogle Scholar
  2. Abiko Y, Sato T, Mayanagi G, Takahashi N (2010) Profiling of subgingival plaque biofilm microflora from periodontally healthy subjects and from subjects with periodontitis using quantitative real-time PCR. J Periodontal Res 45:389–395CrossRefPubMedGoogle Scholar
  3. Anupama R, Mukherjee A, Babu S (2017) Gene-centric metegenome analysis reveals diversity of Pseudomonas aeruginosa biofilm gene orthologs in fresh water ecosystem. Genomics 110:89–87CrossRefPubMedGoogle Scholar
  4. Anupama R, Sajitha LS, Mukherjee A, Babu S (2018) Cross-regulatory network in Pseudomonas aeruginosa biofilm genes and TiO2 anatase induced molecular perturbations in key proteins unraveled by a systems biology approach. Gene 64:289–296CrossRefGoogle Scholar
  5. Babin BM, Bergkessel M, Sweredoskie MJ, Moradiane A, Hesse S, Newman DK, Tirrel DA (2015) SutA is a bacterial transcription factor expressed during slow growth in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 103:2833–2838Google Scholar
  6. Babin BM, Atangcho L, van Eldijk MB, Sweredoski MJ, Moradian A, Hess S, Tolker-Nielsen T, Newman DK, Tirrell DA (2017) Selective proteomic analysis of antibiotic-tolerant cellular subpopulations in Pseudomonas aeruginosa biofilms. mBio 8:e01593–e01517CrossRefPubMedPubMedCentralGoogle Scholar
  7. Basic A, Blomqvist M, Dahlén G, Svensäter G (2017) The proteins of Fusobacterium spp. involved in hydrogen sulfide production from l-cysteine. BMC Microbiol 17:61CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43:345–353CrossRefGoogle Scholar
  9. Carvalhais V, Cerveira F, Vilanova M, Cerca N, Vitorino R (2015) An immunoproteomic approach for characterization of dormancy within Staphylococcus epidermidis biofilms. Mol Immunol 65:429–435CrossRefPubMedGoogle Scholar
  10. Chavez-Dozal A, Gorman C, Nishiguchi MK (2015) Proteomic and metabolomic profiles demonstrate variation among free-living and symbiotic Vibrio fischeri biofilms. BMC Microbiol 215:226CrossRefGoogle Scholar
  11. Chen S, Hao H, Zhao P, Ji W, Li M, Liu Y, Chu Y (2018) Differential immunoreactivity to bovine convalescent serum between Mycoplasma bovis biofilms and planktonic cells revealed by comparative immunoproteomic analysis. Front Microbiol 9:379CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chew J, Zilm SP, Fuss JM, Gully NJ (2012) A proteomic investigation of Fusobacterium nucleatum alkaline-induced biofilms. BMC Microbiol 12:189CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chignell JF, De Long SK, Reardon KF (2018) Meta-proteomic analysis of protein expression distinctive to electricity-generating biofilm communities in air-cathode microbial fuel cells. Biotechnol Biofuels 11:121CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chua SL, Yam JKH, Hao P, Adav SS, Salido MM, Liu Y, Givskov M, Sze SK, Nielsen TT, Yang L (2016) Selective labeling and eradication of antibiotic-tolerant bacterial populations in Pseudomonas aeruginosa biofilms. Nat Commun 7:10750.  https://doi.org/10.1038/ncomms10750 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Clark ME, He Z, Redding AM, Joachimiak MP (2012) Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: carbon and energy flow contribute to the distinct biofilm growth state. BMC Genom 13:138CrossRefGoogle Scholar
  16. Collet A, Cosette P, Beloin C, Ghigo JM, Rihouey C, Lerouge P, Junter GA, Jouenne T (2008) Impact of rpoS deletion on the proteome of Escherichia coli grown planktonically and as biofilm. J Proteome Res 7:4659–4669CrossRefPubMedGoogle Scholar
  17. DeSouza LV, Siu KWM (2013) Mass spectrometry-based quantification. Clin Biochem 46:421–431CrossRefPubMedGoogle Scholar
  18. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA 100:10995–11000CrossRefPubMedGoogle Scholar
  19. Favre L, Ortalo-Magne A, Pichereaux C, Gargaros A, Burlet-Schiltz O, Cotelle V, Culioli G (2018) Metabolome and proteome changes between biofilm and planktonic phenotypes of the marine bacterium Pseudoalteromonas lipolytica TC8. Biofouling 34:132–148CrossRefPubMedGoogle Scholar
  20. Freiberg JA, Le Breton Y, Tran BQ, Scott AJ, Harro JM, Ernst RK, Goo YA, Mongodin EF, Goodlett DR, McIver KS, Shirtliff ME (2016) Global analysis and comparison of the transcriptomes and proteomes of group A Streptococcus biofilms. mSystems 1(6):e00149–e00116CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gelfand MS, Rodionov DA (2008) Comparative genomics and functional annotation of bacterial transporters. Phys Life Rev 5:22–49CrossRefGoogle Scholar
  22. Giaouris E, Samoilis G, Chorianopoulos N, Ercolini D, Nychas GJ (2013) Differential protein expression patterns between planktonic and biofilm cells of Salmonella enterica serovar Enteritidis PT4 on stainless steel surface. Int J Food Microbiol 162:105–113CrossRefPubMedGoogle Scholar
  23. Hamilton S, Bongaerts RJ, Mulholland F, Cochrane B, Porter J, Lucchini S, Lappin-Scott HM, Hinton JCD (2009) The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genom 10:599CrossRefGoogle Scholar
  24. Hansen AM, Qiu Y, Yeh N, Blattner FR, Durfee T, Jin DJ (2005) SspA is required for acid resistance in stationary phase by downregulation of H-NS in Escherichia coli. Mol Microbiol 56:719–734CrossRefPubMedGoogle Scholar
  25. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273CrossRefPubMedGoogle Scholar
  26. Herschend J, Damholt ZBV, Marquard AM, Svensson B, Sørensen SJ, Hägglund P, Burmølle M (2017) A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community. Sci Rep 7(1):16483CrossRefPubMedPubMedCentralGoogle Scholar
  27. Islam N, Kim Y, Ross JM, Marten MR (2014) Proteome analysis of Staphylococcus aureus biofilm cells grown under physiologically relevant fluid shear conditions. Proteome Sci 12:21CrossRefPubMedPubMedCentralGoogle Scholar
  28. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kavanagh P, Botting CH, Jana PS, Leech D, Abram F (2016) Comparative proteomics implicates a role for multiple secretion systems in electrode-respiring Geobacter sulfurreducens biofilms. J Proteome Res 15:4135–4145CrossRefGoogle Scholar
  30. Khemiri A, Jouenne T, Cosette P (2016) Proteomics dedicated to biofilmology: what have we learned from a decade of research? Med Microbiol Immunol 205(1):1–19CrossRefPubMedGoogle Scholar
  31. Kumar D, Mondal AK, Kutum R, Dash D (2016) Proteogenomics of rare taxonomic phyla: a prospective treasure trove of protein coding genes. Proteomics 16:226–240CrossRefPubMedGoogle Scholar
  32. Landgraf P, Antileo ER, Schuman EM, Dieterich DC (2015) BONCAT: metabolic labeling, click chemistry, and affinity purification of newly synthesized proteomes. Methods Mol Biol 1266:199–215CrossRefPubMedGoogle Scholar
  33. Lassek C, Burghartz M, Chaves-Moreno D, Otto A, Hentschker C, Fuchs S, Bernhardt J, Jauregui R, Neubauer R, Becher D, Pieper DH, Jahn M, Jahn D, Riedel K (2015) A metaproteomics approach to elucidate host and pathogen protein expression during catheter-associated urinary tract infections (CAUTIs). Mol Cell Proteom 14(4):989–1008CrossRefGoogle Scholar
  34. Lee JH, Kim YG, Cho MH, Lee J (2014) ZnO nanoparticles inhibit Pseudomonas aeruginosa biofilm formationand virulence factor production. Microbiol Res 169:888–896CrossRefPubMedGoogle Scholar
  35. Li W, Yao Z, Sun L, Hu W, Cao J, Lin W, Lin X (2016) Proteomics analysis reveals a potential antibiotic cocktail therapy strategy for Aeromonas hydrophila infection in biofilm. J Proteome Res 15:1810–1820CrossRefPubMedGoogle Scholar
  36. Lourenço A, de Las Heras A, Scortti M, JVazquez-Boland J, Frank JF, Britoa L (2013) Comparison of Listeria monocytogenes exoproteomes from biofilm and planktonic state: Lmo2504, a protein associated with biofilms. Appl Environ Microbiol 79:6075–6082CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mewborn L, Benitez JA, Silva AJ (2017) Flagellar motility, extracellular proteases and Vibrio cholerae detachment from abiotic and biotic surfaces. Microb Pathog 113:17–24CrossRefPubMedGoogle Scholar
  38. Mikkelsen H, Duck Z, Lilley KS, Welch M (2007) Interrelationships between colonies, biofilms and planktonic cells of Pseudomonas aeruginosa. J Bacteriol 189:2411–2416CrossRefPubMedPubMedCentralGoogle Scholar
  39. Moorthy S, Watnick PI (2004) Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol Microbiol 52:573–587CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mosier AC, Li Z, Thomas BC, Hettich RL, Pan C, Banfield JF (2015) Elevated temperature alters proteomic responses of individual organisms within a biofilm community. ISME J 9:180–194CrossRefPubMedGoogle Scholar
  41. O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304CrossRefPubMedGoogle Scholar
  42. Oosthuizen MC, Steyn B, Lindsay DJ, Brözel VS, Cosette P, von Holy A (2001) Novel method for the proteomic investigation of a dairy-associated Bacillus cereus biofilm. Appl Environ Microbiol 194:47–51Google Scholar
  43. Park AJ, Murphy K, Krieger JR, Brewer D, Taylor P, Habash M, Khursigara CM (2014) A temporal examination of the planktonic and biofilm proteome of whole cell Pseudomonas aeruginosa PAO1 using quantitative mass spectrometry. Mol Cell Proteom 13(4):1095–1105CrossRefGoogle Scholar
  44. Pérez-Ibarreche M, Mendoza LM, Vignolo G, Fadda S (2017) Proteomic and genetics insights on the response of the bacteriocinogenic Lactobacillus sakei CRL1862 during biofilm formation on stainless steel surface at 10 °C. Int J Food Microbiol 3:258:18–27CrossRefGoogle Scholar
  45. Pham TK, Roy S, Noirel J, Douglas I, Wright PC, Stafford GP (2010) A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics 10:313–341CrossRefGoogle Scholar
  46. Pobre V, Arraiano CM (2015) Next generation sequencing analysis reveals that the ribonucleases RNase II, RNase R and PNPase affect bacterial motility and biofilm formation in E. coli. BMC Genom 16:72CrossRefGoogle Scholar
  47. Poirier I, Hammannb P, Kuhnb L, Bertrand M (2013) Strategies developed by the marine bacterium Pseudomonas fluorescens BA3SM1 to resist metals: a proteome analysis. Aquat Toxicol 128–129:215–232CrossRefPubMedGoogle Scholar
  48. Poirier I, Kuhnb L, Demortière A, Mirvaux B, Hammann P, Chicher J, Caplat C, Palluda M, Bertrand M (2016) Ability of the marine bacterium Pseudomonas fluorescens BA3SM1 to counteract the toxicity of CdSe nanoparticles. J Proteom 148:213–227CrossRefGoogle Scholar
  49. Pysz MA, Conners SB, Montero CI, Shockley KR, Johnson MR, Ward DE, Kelly RA (2004) Transcriptional analysis of biofilm formation processes in the anaerobic, hyperthermophilic bacterium Thermotoga maritim. Appl Environ Microbiol 70:6098–6112CrossRefPubMedPubMedCentralGoogle Scholar
  50. Qayyum S, Sharma D, Bisht D, Khan AU (2016) Protein translation machinery holds a key for transition of planktonic cells to biofilm state in Enterococcus faecalis: a proteomic approach. Biochem Biophys Res Commun 474:652–659CrossRefPubMedGoogle Scholar
  51. Qiu M, Xu Z, Li X, Li Q, Zhang N, Shen Q, Zhang R (2014) Comparative proteomics analysis of Bacillus amyloliquefaciens SQR9 revealed the key proteins involved in in situ root colonization. J Proteome Res 13:5581–5591CrossRefPubMedGoogle Scholar
  52. Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97:4885–4890CrossRefPubMedGoogle Scholar
  53. Rathsam C, Eaton RE, Simpson CL, Browne GV, Valova VA, Harty DWS, Jacques NA (2005) Two-dimensional fluorescence difference gel electrophoretic analysis of Streptococcus mutans biofilms. J Proteome Res 4:2161–2173CrossRefPubMedGoogle Scholar
  54. Sadeghinejad L, Cvitkovitch DG, Siqueira WL, Santerre JP, Finer Y (2016) Triethylene glycol up-regulates virulence- associated genes and proteins in Streptococcus mutans. PLoS ONE 11(11):e0165760CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sauer K, Camper AK (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 183:6579–6589CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biolfilm. J Bacteriol 184:1140–1154CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sauer K, Cullen MC, Rickard AH, Zeef LAH, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326CrossRefPubMedPubMedCentralGoogle Scholar
  58. Schembri MA, Kjaergaard K, Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267CrossRefPubMedGoogle Scholar
  59. Schmidt R, Krizsan A, Volke D, Knappe D, Hoffmann R (2016) Identification of new resistance mechanisms in Escherichia Coli against apidaecin 1b using quantitative gel and LC–MS-based proteomics. J Proteome Res 15:2607–2617CrossRefPubMedGoogle Scholar
  60. Sethupathy S, Prasath KG, Ananthi S, Mahalingam S, Balan SY, Pandian SK (2016) Proteomic analysis reveals modulation of iron homeostasis and oxidative stress response in Pseudomonas aeruginosa PAO1 by curcumin inhibiting quorum sensing regulated virulence factors and biofilm production. J Proteom 145:112–126CrossRefGoogle Scholar
  61. Shao C, Sun Y, Wang N, Yu H, Zhou Y, Chen C, Jia J (2013) Changes of proteome components of Helicobacter pylori biofilms induced by serum starvation. Mol Med Rep 8:1761–1766CrossRefPubMedGoogle Scholar
  62. Shemesh M, Tam A, Steinberg D (2007) Differential gene expression profiling of Streptococcus mutan cultured under biofilm and planktonic conditions. Microbiol 153:1307–1317CrossRefGoogle Scholar
  63. Silva MS, De Souza AA, Takita MA, Labate CA, Machado MA (2011) Analysis of the biofilm proteome of Xylella fastidiosa. Proteome Sci 9:58CrossRefPubMedPubMedCentralGoogle Scholar
  64. Silva AF, Dos Santos AR, Coelho Trevisan DA, Ribeiro AB, Zanetti Campanerut-Sá PA, Kukolj C, de Souza EM, Cardoso RF, Estivalet Svidzinski TI, de Abreu Filho BA, Junior MM, Graton Mikcha JM (2018) Cinnamaldehyde induces changes in the protein profile of Salmonella Typhimurium biofilm. Res Microbiol 169:33–43CrossRefPubMedGoogle Scholar
  65. Soares A, Gomes LC, Mergulhao FJ (2018) Comparing the recombinant protein production potential of planktonic and biofilm cells. Microorganisms 6:48.  https://doi.org/10.3390/microorganisms6020048 CrossRefPubMedCentralGoogle Scholar
  66. Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951–1957CrossRefPubMedPubMedCentralGoogle Scholar
  67. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199CrossRefPubMedGoogle Scholar
  68. Sun L, Chen H, Lin W, Lin X (2017) Quantitative proteomic analysis of Edwardsiella tarda in response to oxytetracycline stress in biofilm. J Proteom 150:141–148CrossRefGoogle Scholar
  69. Sze SK, Nielsen TT, Yang L (2016) Selective labelling and eradication of antibiotictolerant bacterial populations in Pseudomonas aeruginosa biofilms. Nat Commun 7:10750CrossRefPubMedPubMedCentralGoogle Scholar
  70. Toyofuku M, Roschitzki B, Riedel K, Eberl L (2012) Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix. J Proteome Res 11:4906–4915CrossRefPubMedGoogle Scholar
  71. Tremoulet F, Duche O, Namane A, Martinie B, Labadie JC (2002) Comparison of protein patterns of Listeria monocytogenes grown in biofilm or in planktonic mode by proteome analysis. FEMS Microbiol Lett 210:25–31CrossRefPubMedGoogle Scholar
  72. Van Alen T, Claus H, Zahedi RP, Groh J, Blazyca H, Lappann M, Sickmann A, Vogel U (2010) Comparative proteomic analysis of biofilm and planktonic cells of Neisseria meningitides. Proteomics 24:4512–4521CrossRefGoogle Scholar
  73. Vaysse PJ, Prat L, Mangenot S, Cruveiller S, Goulas P, Grimaud R (2009) Proteomic analysis of Marinobacter hydrocarbonoclasticus SP17 biofilm formation at the alkane-water interface reveals novel proteins and cellular processes involved in hexadecane assimilation. Res Microbiol 160:829–837CrossRefPubMedGoogle Scholar
  74. Wang Y, Yi L, Wu Z, Shao J, Liu G (2012) Comparative proteomic analysis of Streptococcus suis biofilms and planktonic cells that identified biofilm infection-related immunogenic proteins. PLoS ONE  https://doi.org/10.1371/journal.pone.0033371 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wang DZ, Kong LF, Li YY, Xie ZX (2016) Environmental microbial community proteomics: status, challenges and perspectives. Int J Mol Sci 17(8):1275CrossRefPubMedCentralGoogle Scholar
  76. Weber A, Kögl SA, Jung K (2006) Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J Bacteriol 188:7165–7175CrossRefPubMedPubMedCentralGoogle Scholar
  77. Wick LM, Quadroni M, Egli T (2001) Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucose-limited growth conditions in continuous culture and vice versa. Environ Microbiol 3:588–599CrossRefPubMedGoogle Scholar
  78. Williams MD, Ouyang TX, Flickinger MC (1994) Starvation-induced expression of SspA and SspB: the effects of a null mutation in sspA on Escherichia coli protein synthesis and survival during growth and prolonged starvation. Mol Microbiol 11:1029–1043CrossRefPubMedGoogle Scholar
  79. Wood TK, Hong SH, Qun M (2010) Engineering biofilm formation and dispersal. Trends Biotechnol 29:87–94CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.School of Biosciences and TechnologyVIT UniversityVelloreIndia

Personalised recommendations