Skip to main content
SpringerLink
Log in

Evaluation of the differences between biofilm and planktonic Brucella abortus via metabolomics and proteomics

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

This study analyzed the difference between biofilm and planktonic Brucella abortus using metabolomics and proteomics. Brucella abortus was cultured in different media to induce Brucella abortus biofilm formation and planktonic cells, followed by metabolomics and proteomics analyses for these two samples. Significant differential metabolites were identified, followed by KEGG pathway analysis. Differentially expressed proteins were identified, followed by subcellular localization, GO annotation, and KEGG pathway enrichment. Additionally, a correlation analysis of metabolomics and proteomics was performed. Metabolomics analysis showed 7682 positive and 4433 negative metabolites, including 188 positive and 117 negative significant differential metabolites. These differential metabolites were enriched in fatty acid/unsaturated fatty acid biosynthesis and linoleic acid metabolism. Proteomics analysis revealed 1759 proteins, including 486 differentially expressed proteins, which were enriched in various metabolic and degradation-related pathways. Subcellular localization showed that 74.3% of the differential proteins were cytoplasmic proteins. Correlation analysis showed that 1-palmitoyl-2-oleoyl-phosphatidylglycerol had the most significant correlations with proteins, followed by cytosine. Both metabolites correlated with the protein Q57EI7 (RbsB-1, ribose ABC transporter). One common pathway, fatty acid biosynthesis, was identified by both proteomics and metabolomics analyses that involved the metabolites, oleic acid, and protein Q57DK3 (biotin carboxylase). There were metabolomic and proteomic differences between Brucella abortus biofilm and planktonic cells, and these results provide novel insights into the biofilm-forming process of Brucella abortus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Almirón MA, Roset MS, Sanjuan N (2013) The aggregation of Brucella abortus occurs under microaerobic conditions and promotes desiccation tolerance and biofilm formation. The open microbiology journal 7:87–91

    Article  Google Scholar 

  • Brylinski M, Waldrop GL (2014) Computational redesign of bacterial biotin carboxylase inhibitors using structure-based virtual screening of combinatorial libraries. Molecules (Basel, Switzerland) 19:4021–4045

    Article  Google Scholar 

  • Cai JN, Kim MA, Jung JE, Pandit S, Song KY, Jeon JG (2015) Effects of combined oleic acid and fluoride at sub-MIC levels on EPS formation and viability of Streptococcus mutans UA159 biofilms. Biofouling 31:555–563

    Article  CAS  Google Scholar 

  • Carvalhais V, França A, Pier GB, Vilanova M, Cerca N, Vitorino R (2015) Comparative proteomic and transcriptomic profile of Staphylococcus epidermidis biofilms grown in glucose-enriched medium. Talanta 132:705–712

    Article  CAS  Google Scholar 

  • Chao J, Wolfaardt GM, Arts MT (2010) Characterization of Pseudomonas aeruginosa fatty acid profiles in biofilms and batch planktonic cultures. Can J Microbiol 56:1028–1039

    Article  CAS  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics (Oxford, England) 21:3674–3676

    Article  CAS  Google Scholar 

  • Dubois-Brissonnet F (2019) Characterization of bacterial membrane fatty acid profiles for biofilm cells. Methods Mol Biol 1918:165–170

    Article  CAS  Google Scholar 

  • Fadhlaoui M, Laderriere V, Lavoie I, Fortin C (2020) Influence of temperature and nickel on algal biofilm fatty acid composition. Environ Toxicol Chem 39:1566–1577

    Article  CAS  Google Scholar 

  • Favre L, Ortalo-Magné A, Greff S, Pérez T, Thomas OP, Martin JC, Culioli G (2017) Discrimination of four marine biofilm-forming bacteria by LC-MS metabolomics and influence of culture parameters. Journal of proteome research 16:1962–1975

    Article  CAS  Google Scholar 

  • 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. Scientific reports 7:16483–16483

    Article  Google Scholar 

  • Kanehisa M, Sato Y (2020) KEGG Mapper for inferring cellular functions from protein sequences. Protein science : a publication of the Protein Society 29:28–35

    Article  CAS  Google Scholar 

  • Kaur A, Capalash N, Sharma P (2018) Quorum sensing in thermophiles: prevalence of autoinducer-2 system. BMC Microbiol 18:62

    Article  Google Scholar 

  • Kim SK, Lee JH (2016) Biofilm dispersion in Pseudomonas aeruginosa. Journal of microbiology (Seoul, Korea) 54:71–85

    CAS  Google Scholar 

  • Lu H, Que Y, Wu X, Guan T, Guo H (2019) Metabolomics deciphered metabolic reprogramming required for biofilm formation. Scientific reports 9:13160

    Article  Google Scholar 

  • Muthamil S, Prasath KG, Priya A, Precilla P, Pandian SK (2020) Global proteomic analysis deciphers the mechanism of action of plant derived oleic acid against Candida albicans virulence and biofilm formation. Sci Rep 10:5113

    Article  CAS  Google Scholar 

  • Novak EA, Shao H, Daep CA, Demuth DR (2010) Autoinducer-2 and QseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans. Infect Immun 78:2919–2926

    Article  CAS  Google Scholar 

  • Pisithkul, T., Schroeder, J.W., Trujillo, E.A., Yeesin, P., Stevenson, D.M., Chaiamarit, T., et al (2019a). Metabolic remodeling during biofilm development of Bacillus subtilis. mBio 10.

  • Pisithkul T, Schroeder JW, Trujillo EA, Yeesin P, Stevenson DM, Chaiamarit T et al (2019b) Metabolic remodeling during biofilm development of Bacillus subtilis. mBio 10:e00623–e00619

    Article  CAS  Google Scholar 

  • Sadiq FA, Flint S, Li Y, Liu T, Lei Y, Sakandar HA, He GQ (2017) New mechanistic insights into the motile-to-sessile switch in various bacteria with particular emphasis on Bacillus subtilis and Pseudomonas aeruginosa: a review. Biofouling 33:306–326

    Article  CAS  Google Scholar 

  • Shao H, Lamont RJ, Demuth DR (2007) Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect Immun 75:4211–4218

    Article  CAS  Google Scholar 

  • Skagia A, Zografou C, Vezyri E, Venieraki A, Katinakis P, Dimou M (2016) Cyclophilin PpiB is involved in motility and biofilm formation via its functional association with certain proteins. Genes Cells 21:833–851

    Article  CAS  Google Scholar 

  • Stenz L, François P, Fischer A, Huyghe A, Tangomo M, Hernandez D et al (2008) Impact of oleic acid (cis-9-octadecenoic acid) on bacterial viability and biofilm production in Staphylococcus aureus. FEMS Microbiol Lett 287:149–155

    Article  CAS  Google Scholar 

  • Suárez-Esquivel M, H.-M. G, Ruiz-Villalobos N, Barquero-Calvo E, Chacón-Díaz C, Ladner JT, Oviedo-Sánchez G, Foster JT, Rojas-Campos N, Chaves-Olarte E, Thomson NR, Moreno E, Guzmán-Verri C (2020) Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis. PLoS Negl Trop Dis 14:e0008235

    Article  Google Scholar 

  • Suriyanarayanan T, Qingsong L, Kwang LT, Mun LY, Truong T, Seneviratne CJ (2018) Quantitative proteomics of strong and weak biofilm formers of Enterococcus faecalis reveals novel regulators of biofilm formation. Molecular & cellular proteomics : MCP 17:643–654

    Article  CAS  Google Scholar 

  • Suryaletha K, Narendrakumar L, John J, Radhakrishnan MP, George S, Thomas S (2019) Decoding the proteomic changes involved in the biofilm formation of Enterococcus faecalis SK460 to elucidate potential biofilm determinants. BMC microbiology 19:146

    Article  Google Scholar 

  • Tang T, Chen G, Guo A, Xu Y, Zhao L, Wang M, Lu C, Jiang Y, Zhang C (2020) Comparative proteomic and genomic analyses of Brucella abortus biofilm and planktonic cells. Molecular medicine reports 21:731–743

    CAS  PubMed  Google Scholar 

  • Wiśniewski JR, Mann M (2016) A proteomics approach to the protein normalization problem: selection of unvarying proteins for MS-based proteomics and western blotting. Journal of proteome research 15:2321–2326

    Article  Google Scholar 

  • Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nature methods 6:359–362

    Article  Google Scholar 

  • Yin W, Wang Y, Liu L, He J (2019) Biofilms: the microbial "protective clothing" in extreme environments. International journal of molecular sciences 20:3423

    Article  CAS  Google Scholar 

  • Zhang B, Powers R (2012) Analysis of bacterial biofilms using NMR-based metabolomics. Future Med Chem 4:1273–1306

    Article  CAS  Google Scholar 

Download references

Availability of data and materials

Not applicable. This study was only the primary research, and further studies are in progress.

Funding

This study was supported by the National Natural Science Foundation of China (No. 31702278), the Fundamental Research Funds for the Central Universities (No. KYDS201801, KJQN201826), the Science Foundation of General Administration of Customs of the People’s Republic of China (No. 2019HK018), and the Science Foundation of General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China (No. 2008IK004). The role of funders is financially supporting this study.

Author information

Authors and Affiliations

  1. Animal, Plant and Food Inspection Center, Nanjing Customs District, Nanjing, Jiangsu Province, 210001, People’s Republic of China

    Taishan Tang, Xiao Tan, Xiaona Zhao & Ping Zhou

  2. MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Xuanwu, Nanjing, Jiangsu Province, 210095, People’s Republic of China

    Taishan Tang, Chengping Lu & Huixing Lin

  3. Lianyungang Customs Comprehensive Technology Center, Nanjing Customs District, Lianyungang, Jiangsu, 222000, People’s Republic of China

    Ye Xu

  4. Technical Centre of Ningbo Customs, Ningbo Customs District, Ningbo, Zhejiang Province, 315100, People’s Republic of China

    Jianfeng Wang

  5. Technical Center, Xiamen Customs District, Xiamen, Fujian, 361026, People’s Republic of China

    Fande Kong

  6. School of Food Science, Nanjing Xiaozhuang University, Nanjing, Jiangsu Province, 211171, People’s Republic of China

    Changqing Zhu

Authors
  1. Taishan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ye Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaona Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fande Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Changqing Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chengping Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Huixing Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Tang and Lu conceived and designed the research, and Ye Xu and Jianfeng Wang participated in the acquisition of data. Xiao Tan and Xiaona Zhao analyzed and interpreted the data. Zhou and Fande Kong participated in the design of the study and performed the statistical analyses. Changqing Zhu and Huixing Lin conceived the study and participated in its design and coordination; Taishan Tang and Chengping Lu drafted the manuscript and revised the manuscript for important intellectual content. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Chengping Lu.

Ethics declarations

Ethics approval

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

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

Supplementary information

Supplementary Figure 1

Correlation analysis of the differentially expressed metabolites in biofilm and planktonic stage (PNG 535 kb)

High Resolution Image (TIF 2125 kb)

Table S1.

Identification of metabolites at positive mode. (XLSX 2493 kb)

Table S2.

Identification of metabolites at negative mode. (XLSX 1100 kb)

Table S3.

Results for proteins identification. (XLSX 333 kb)

Table S4.

Results for subcellular localization. (XLSX 16 kb)

Table S5.

The significant metabolite-protein interaction pairs in Pearson correlation analysis. (XLS 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, T., Xu, Y., Wang, J. et al. Evaluation of the differences between biofilm and planktonic Brucella abortus via metabolomics and proteomics. Funct Integr Genomics 21, 421–433 (2021). https://doi.org/10.1007/s10142-021-00788-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-021-00788-7

Keywords

Search

Navigation