Skip to main content

Advertisement

SpringerLink
Log in

Antibacterial activity and lantibiotic post-translational modification genes in Streptococcus spp. isolated from ruminal fluid

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

The production of bacteriocins is frequently described in high microbial diversity environments. The aims of this study were to screen Streptococcus spp. isolated from rumen for their antibacterial potential and to determine the presence of post-translational modification genes for lantibiotic class of bacteriocins. The isolates were tested for production of antibacterial compounds by the spot-on-lawn assay. Presence of interfering factors and the sensitivity to proteinase K were evaluated. The ruminal bacteria were identified by 16S rRNA gene sequencing and the subspecific discrimination of the isolates belonging to the same specie was performed by PFGE. The presence of lantibiotic post-translational modification genes (lanB, lanC, and lanM) into bacterial genomes was performed by PCR. The bacteriocin-like inhibitory substances showed broad inhibitory activity and the producer cells were identified as S. equinus, S. lutetiensis, and S. gallolyticus. According to PFGE, the isolates identified as S. equinus belong to different strains. Three ruminal isolates showed at least one of the lantibiotic post-translational modification genes, and lanC was more frequently detected (75%). The production of broad-spectrum bacteriocin-like inhibitory substances by rumen strains suggests that antimicrobial peptides may play an important role in competition in the complex ruminal ecosystem.

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

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 5:403–410

    Article  Google Scholar 

  • Alvarez-Sieiro P, Montalbán-López M, Mu D et al (2016) Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 100:2939–2951

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Barbosa AA, Mantovani HC, Jain S (2017) Bacteriocins from lactic acid bacteria and their potential in the preservation of fruit products. Crit Rev Biotechnol 3:1–13

    Google Scholar 

  • Benson JA, Ferrieri P (2001) Rapid pulsed-field gel electrophoresis method for group B streptococcus isolates. J Clin Microbiol 39:3006–3008

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Booth SJ, Johnson JL, Wilkins TD (1977) Bacteriocin production by strains of Bacteroides isolated from human feces and the role of these strains in the bacterial ecology of the colon. Antimicrob Agents Chemother 11:718–724

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chakchouk-Mtibaa A, Elleuch L, Smaoui S et al (2014) An antilisterial bacteriocin BacFL31 produced by Enterococcus faecium FL31 with a novel structure containing hydroxyproline residues. Anaerobe 27:1–6

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Hoover DG (2003) Bacteriocins and their food applications. Compr Rev Food Sci Food Saf 2:82–100

    CAS  Google Scholar 

  • Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacterioicns: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20

    Article  PubMed  CAS  Google Scholar 

  • Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788

    Article  PubMed  CAS  Google Scholar 

  • Diep DB, Nes IF (2002) Ribosomally synthesized antibacterial peptides in Gram positive bacteria. Curr Drug Targets 3:107–122

    Article  PubMed  CAS  Google Scholar 

  • Drider D, Bendali F, Naghmouchi K et al (2016) Bacteriocins: not only antibacterial agents. Probiotics Antimicrob Proteins 8:177–182

    Article  PubMed  CAS  Google Scholar 

  • Escano J, Stauffer B, Brennan J et al (2015) Biosynthesis and transport of the lantibiotic mutacin 1140 produced by Streptococcus mutans. J Bacteriol 197:1173–1184

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Espeche MC, Otero MC, Sesma F et al (2009) Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet Microbiol 135:346–357

    Article  PubMed  CAS  Google Scholar 

  • Hillman JD, Novák J, Sagura E et al (1998) Genetic and biochemical analysis of mutacin 1140, a lantibiotic from Streptococcus mutans. Infect Immun 66:2743–2749

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hyink O, Balakrishnan M, Tagg JR (2005) Streptococcus rattus strain BHT produces both a class I two-component lantibiotic and a class II bacteriocin. FEMS Microbiol Lett 252:235–241

    Article  PubMed  CAS  Google Scholar 

  • Joachimsthal EL, Reeves RK, Hung J et al (2010) Production of bacteriocins by Streptococcus bovis strains from Australian ruminants. J Appl Microbiol 108:428–436

    Article  PubMed  CAS  Google Scholar 

  • Joerger RD (2003) Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poult Sci 82:640–647

    Article  PubMed  CAS  Google Scholar 

  • Kabuki T, Kawai Y, Uenishi H et al (2011) Gene cluster for biosynthesis of thermophilin 1277--a lantibiotic produced by Streptococcus thermophilus SBT1277, and heterologous expression of TepI, a novel immunity peptide. J Appl Microbiol 110:641–649

    Article  PubMed  CAS  Google Scholar 

  • Kalmokoff ML, Cyr TD, Hefford MA et al (2003) Butyrivibriocin AR10, a new cyclic bacteriocin produced by the ruminal anaerobe Butyrivibrio fibrosolvens AR10: characterization of the gene and peptide. Can J Microbiol 49:763–773

    Article  PubMed  CAS  Google Scholar 

  • Kaškonienė V, Stankevičius M, Bimbiraitė-Survilienė K et al (2017) Current state of purification, isolation and analysis of bacteriocins produced by lactic acid bacteria. Appl Microbiol Biotechnol 101:1323–1335

    Article  PubMed  CAS  Google Scholar 

  • Kisidayová S, Lauková A, Jalc D (2009) Comparison of nisin and monensin effects on ciliate and selected bacterial populations in artificial rumen. Folia Microbiol 54:527–532

    Article  CAS  Google Scholar 

  • Li SW, Chen YS, Lee YS et al (2017) Comparative genomic analysis of bacteriocin-producing Weissella cibaria 110. Appl Microbiol Biotechnol 101:1227–1237

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Xiang Q, Zhang Q et al (2012) Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37:207–215

    Article  PubMed  CAS  Google Scholar 

  • Mantovani HC, Kam DK, Ha JK et al (2001) The antibacterial activity and sensitivity of Streptococcus bovis strains isolated from the rumen of cattle. FEMS Microbial Ecol 37:223–229

    CAS  Google Scholar 

  • Mantovani HC, Russell JB (2002) The ability of a bacteriocin of Streptococcus bovis HC5 (bovicin HC5) to inhibit Clostridium aminophilum, an obligate amino acid fermenting bacterium from the rumen. Anaerobe 8:247–252

    Article  CAS  Google Scholar 

  • Mantovani HC, Hu H, Worobo RW et al (2002) Bovicin HC5, a bacteriocin from Streptococcus bovis HC5. Microbiology 148:3347–3352

    Article  PubMed  CAS  Google Scholar 

  • McAuliffe O, Ryan MP, Ross RP et al (1998) Lacticin 3147, a broad-spectrum bacteriocin which selectively dissipates the membrane potential. Appl Environ Microbiol 64:439–445

  • Moraes PM, Perin LM, Todorov SD et al (2012) Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese. J Appl Microbiol 113:318–328

    Article  PubMed  CAS  Google Scholar 

  • Oliveira SD, Santos LR, Schuch DM et al (2002) Detection and identification of salmonellas from poultry-related samples by PCR. Vet Microbiol 87:25–35

    Article  PubMed  CAS  Google Scholar 

  • Ortolani MB, Moraes PM, Perin LM et al (2010) Molecular identification of naturally occurring bacteriocinogenic and bacteriocinogenic-like lactic acid bacteria in raw milk and soft cheese. J Dairy Sci 93:2880–2886

    Article  PubMed  CAS  Google Scholar 

  • Perin LM, Nero LA (2014) Antagonistic lactic acid bacteria isolated from goat milk and identification of a novel nisin variant Lactococcus lactis. BMC Microbiol 14:1–9

    Article  CAS  Google Scholar 

  • Rodriguez E, Gonzalez B, Gaya P et al (2000) Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J 10:7–15

    Article  CAS  Google Scholar 

  • Russell JB, Mantovani HC (2002) The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J Mol Microbiol Biotechnol 4:347–355

    PubMed  CAS  Google Scholar 

  • Russell JB, Strobel HJ (1989) Effect of ionophores on ruminal fermentation. Appl Environ Microbiol 55:1–6

    PubMed  CAS  PubMed Central  Google Scholar 

  • Settani L, Corsetti A (2008) Application of bacteriocins in vegetable food preservation. Int J Food Microbiol 121:123–138

    Article  CAS  Google Scholar 

  • Suzuki M, Rappe MS, Giovannoni SJ (1998) Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64:4522–4529

    PubMed  CAS  PubMed Central  Google Scholar 

  • Turner JW, Jordan HV (1981) Bacteriocin–like activity within the genus Actinomyces. J Dental Res 60:1000–1007

    Article  CAS  Google Scholar 

  • Vaillancourt K, LeBel G, Frenette M et al (2015) Suicin 3908, a new lantibiotic produced by a strain of Streptococcus suis serotype 2 isolated from a healthy carrier pig. PLoS One 10:e0117245

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang HT, Chen IH, Hsu JT (2012) Production and characterization of a bacteriocin from ruminal bacterium Ruminococcus albus 7. Biosci Biotechnol Biochem 76:34–41

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Ma H, Ge X et al (2014) Bovicin HJ50-like lantibiotics, a novel subgroup of lantibiotics featured by an indispensable disulfide bridge. PLoS One 9:e97121

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wescombe PA, Dyet KH, Dierksen KP et al (2012) Salivaricin G32, a homolog of the prototype Streptococcus pyogenes nisin-like lantibiotic SA-FF22, produced by the commensal species Streptococcus salivarius. Int J Microbiol 2012:1–10

    Article  CAS  Google Scholar 

  • Whitford MF, McPherson MA, Forster RJ et al (2001) Identification of bacteriocin-like inhibitors from rumen Streptococcus spp. and isolation and characterization of bovicin 255. Appl Environ Microbiol 67:569–574

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wirawan RE, Klesse NA, Jack RW et al (2006) Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis. Appl Environ Microbiol 72:1148–1156

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yi H, Zhang L, Tuo Y et al (2010) A novel method for rapid detection of class IIa bacteriocin-producing lactic acid bacteria. Food Control 21:426–430

    Article  CAS  Google Scholar 

  • Zhao X, van der Donk WA (2016) Structural characterization and bioactivity analysis of the two-component lantibiotic Flv system from a ruminant bacterium. Cell Chem Biol 18:246–256

    Article  CAS  Google Scholar 

  • Zou W, Chen HC, Hise KB et al (2013) Meta-analysis of pulsed-field gel electrophoresis fingerprints based on a constructed Salmonella database. PLoS One 8:e59224

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zou W, Lin WJ, Foley SL et al (2010) Evaluation of pulsed-field gel electrophoresis profiles for identification of Salmonella serotypes. J Clin Microbiol 48:3122–3126

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by Minas Gerais State Funding Agency (FAPEMIG) and Brazilian National Council for Scientific and Technological Development (CNPq).

Author information

Authors and Affiliations

  1. Faculdade de Farmácia, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, Brazil

    Yasmin Neves Vieira Sabino, Romário Costa Fochat & Humberto Moreira Húngaro

  2. Embrapa Gado de Leite, Embrapa, Juiz de Fora, Minas Gerais, Brazil

    Junior Cesar Fernandes Lima, Marlice Teixeira Ribeiro, Pedro Braga Arcuri, Jailton da Costa Carneiro, Marco Antônio Machado, Daniele Ribeiro de Lima Reis & João Batista Ribeiro

  3. Instituto de Ciências Biológicas e Naturais, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil

    Alessandra Barbosa Ferreira Machado & Aline Dias Paiva

Authors
  1. Yasmin Neves Vieira Sabino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Romário Costa Fochat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junior Cesar Fernandes Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marlice Teixeira Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pedro Braga Arcuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jailton da Costa Carneiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marco Antônio Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daniele Ribeiro de Lima Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alessandra Barbosa Ferreira Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Humberto Moreira Húngaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. João Batista Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Aline Dias Paiva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aline Dias Paiva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sabino, Y.N.V., Fochat, R.C., Lima, J.C.F. et al. Antibacterial activity and lantibiotic post-translational modification genes in Streptococcus spp. isolated from ruminal fluid. Ann Microbiol 69, 131–138 (2019). https://doi.org/10.1007/s13213-018-1407-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-018-1407-2

Keywords

Search

Navigation