Integration of Transcriptome and Metabolome Reveals the Genes and Metabolites Involved in Biofilm Formation

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2021 Jul 24

PMID 34299216

Citations 14

Authors

Zongmin Liu

Lingzhi Li

Zhifeng Fang

Yuankun Lee

Jianxin Zhao

Hao Zhang

Wei Chen

Haitao Li

Wenwei Lu

Affiliations

Soon will be listed here.

Abstract

strains, an important component of probiotic foods, can form biofilms on abiotic surfaces, leading to increased self-resistance. However, little is known about the molecular mechanism of biofilm formation. A time series transcriptome sequencing and untargeted metabolomics analysis of both biofilm and planktonic cells was performed to identify key genes and metabolites involved in biofilm formation. Two hundred thirty-five nonredundant differentially expressed genes (DEGs) (including , , , , , , , and ) and 219 nonredundant differentially expressed metabolites (including L-threonine, L-cystine, L-tyrosine, ascorbic acid, niacinamide, butyric acid and sphinganine) were identified. Thirteen pathways were identified during the integration of both transcriptomics and metabolomics data, including ABC transporters; quorum sensing; two-component system; oxidative phosphorylation; cysteine and methionine metabolism; glutathione metabolism; glycine, serine and threonine metabolism; and valine, leucine and isoleucine biosynthesis. The DEGs that relate to the integration pathways included , , , , , , , , , , , and . The differentially accumulated metabolites included L-cystine, L-serine, L-threonine, L-tyrosine, methylmalonate, monodehydroascorbate, nicotinamide, orthophosphate, spermine and tocopherol. These results indicate that quorum sensing, two-component system and amino acid metabolism are essential during biofilm formation.

Citing Articles

Integrated Metabolomics and Transcriptomics Analyses Identify Key Amino Acid Metabolic Mechanisms in SMN-LBK.

Shen J, Du Y, Shen Y, Kang N, Fan Z, Fang Z Foods. 2025; 14(5).

PMID: 40077433 PMC: 11899468. DOI: 10.3390/foods14050730.

Type II Toxin-Antitoxin Systems in .

Zhang H, Tao S, Chen H, Fang Y, Xu Y, Han A Infect Drug Resist. 2025; 18:1083-1096.

PMID: 40027916 PMC: 11869752. DOI: 10.2147/IDR.S501485.

Combined Analysis of Transcriptomes and Metabolomes Reveals Key Genes and Substances That Affect the Formation of a Multi-Species Biofilm by Nine Gut Bacteria.

Zhang T, Pei Z, Wang H, Zhao J, Chen W, Lu W Microorganisms. 2025; 13(2).

PMID: 40005603 PMC: 11857192. DOI: 10.3390/microorganisms13020234.

Gut microbiota determines the fate of dietary fiber-targeted interventions in host health.

Wang W, Fan Z, Yan Q, Pan T, Luo J, Wei Y Gut Microbes. 2024; 16(1):2416915.

PMID: 39418223 PMC: 11487953. DOI: 10.1080/19490976.2024.2416915.

Roseburia intestinalis-derived extracellular vesicles ameliorate colitis by modulating intestinal barrier, microbiome, and inflammatory responses.

Han H, Hwang S, Choi S, Hitayezu E, Humphrey M, Enkhbayar A J Extracell Vesicles. 2024; 13(8):e12487.

PMID: 39166405 PMC: 11336657. DOI: 10.1002/jev2.12487.

References

Hofbauer B, Vomacka J, Stahl M, Korotkov V, Jennings M, Wuest W . Dual Inhibitor of Staphylococcus aureus Virulence and Biofilm Attenuates Expression of Major Toxins and Adhesins. Biochemistry. 2018; 57(11):1814-1820. PMC: 6462815. DOI: 10.1021/acs.biochem.7b01271. View

Azeredo J, Azevedo N, Briandet R, Cerca N, Coenye T, Costa A . Critical review on biofilm methods. Crit Rev Microbiol. 2016; 43(3):313-351. DOI: 10.1080/1040841X.2016.1208146. View

Speranza B, Liso A, Russo V, Corbo M . Evaluation of the Potential of Biofilm Formation of subsp. and as Competitive Biocontrol Agents Against Pathogenic and Food Spoilage Bacteria. Microorganisms. 2020; 8(2). PMC: 7074751. DOI: 10.3390/microorganisms8020177. View

Liu J, Martinez-Corral R, Prindle A, Lee D, Larkin J, Gabalda-Sagarra M . Coupling between distant biofilms and emergence of nutrient time-sharing. Science. 2017; 356(6338):638-642. PMC: 5645014. DOI: 10.1126/science.aah4204. View

Sanchez B, Ruiz L, Gueimonde M, Ruas-Madiedo P, Margolles A . Adaptation of bifidobacteria to the gastrointestinal tract and functional consequences. Pharmacol Res. 2012; 69(1):127-36. DOI: 10.1016/j.phrs.2012.11.004. View

Ushakova N, Abramov V, Khlebnikov V, Semenov A, Kuznetsov B, Kozlova A . Properties of the Probiotic Strain Lactobacillus plantarum 8-RA-3 Grown in a Biofilm by Solid Substrate Cultivation Method. Probiotics Antimicrob Proteins. 2016; 4(3):180-6. DOI: 10.1007/s12602-012-9106-y. View

Niederdorfer R, Besemer K, Battin T, Peter H . Ecological strategies and metabolic trade-offs of complex environmental biofilms. NPJ Biofilms Microbiomes. 2017; 3:21. PMC: 5612939. DOI: 10.1038/s41522-017-0029-y. View

Liu C, Sun D, Zhu J, Liu W . Two-Component Signal Transduction Systems: A Major Strategy for Connecting Input Stimuli to Biofilm Formation. Front Microbiol. 2019; 9:3279. PMC: 6335343. DOI: 10.3389/fmicb.2018.03279. View

Turroni F, Duranti S, Milani C, Lugli G, Van Sinderen D, Ventura M . : A Key Member of the Early Human Gut Microbiota. Microorganisms. 2019; 7(11). PMC: 6920858. DOI: 10.3390/microorganisms7110544. View

10.

Munusamy K, Loke M, Vadivelu J, Tay S . LC-MS analysis reveals biological and metabolic processes essential for Candida albicans biofilm growth. Microb Pathog. 2020; 152:104614. DOI: 10.1016/j.micpath.2020.104614. View

11.

Wong E, Ng C, Goh K, Vadivelu J, Ho B, Loke M . Metabolomic analysis of low and high biofilm-forming Helicobacter pylori strains. Sci Rep. 2018; 8(1):1409. PMC: 5780479. DOI: 10.1038/s41598-018-19697-0. View

12.

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

13.

Barzegari A, Kheyrolahzadeh K, Hosseiniyan Khatibi S, Sharifi S, Memar M, Zununi Vahed S . The Battle of Probiotics and Their Derivatives Against Biofilms. Infect Drug Resist. 2020; 13:659-672. PMC: 7049744. DOI: 10.2147/IDR.S232982. View

14.

Oh E, Kim J, Jeon B . Stimulation of biofilm formation by oxidative stress in Campylobacter jejuni under aerobic conditions. Virulence. 2016; 7(7):846-51. PMC: 5029310. DOI: 10.1080/21505594.2016.1197471. View

15.

Zuo F, Yu R, Xiao M, Khaskheli G, Sun X, Ma H . Transcriptomic analysis of Bifidobacterium longum subsp. longum BBMN68 in response to oxidative shock. Sci Rep. 2018; 8(1):17085. PMC: 6244367. DOI: 10.1038/s41598-018-35286-7. View

16.

Bossu M, Selan L, Artini M, Relucenti M, Familiari G, Papa R . Characterization of Biofilm by Original Scanning Electron Microscopy Protocol. Microorganisms. 2020; 8(6). PMC: 7355790. DOI: 10.3390/microorganisms8060807. View

17.

Suzuki I, Shimizu T, Senpuku H . Role of SCFAs for Fimbrillin-Dependent Biofilm Formation of . Microorganisms. 2018; 6(4). PMC: 6313811. DOI: 10.3390/microorganisms6040114. View

18.

Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J . STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2014; 43(Database issue):D447-52. PMC: 4383874. DOI: 10.1093/nar/gku1003. View

19.

Heberle H, Meirelles G, da Silva F, Telles G, Minghim R . InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. 2015; 16:169. PMC: 4455604. DOI: 10.1186/s12859-015-0611-3. View

20.

Saville R, Rakshe S, Haagensen J, Shukla S, Spormann A . Energy-dependent stability of Shewanella oneidensis MR-1 biofilms. J Bacteriol. 2011; 193(13):3257-64. PMC: 3133257. DOI: 10.1128/JB.00251-11. View