Immunomodulatory effects of bacteriocinogenic and non-bacteriocinogenic Lactococcus cremoris of aquatic origin on rainbow trout (Oncorhynchus mykiss, Walbaum)

Front Immunol. 2023 Apr 20:14:1178462. doi: 10.3389/fimmu.2023.1178462. eCollection 2023.

Abstract

Lactic Acid Bacteria (LAB) are a group of bacteria frequently proposed as probiotics in aquaculture, as their administration has shown to confer positive effects on the growth, survival rate to pathogens and immunological status of the fish. In this respect, the production of antimicrobial peptides (referred to as bacteriocins) by LAB is a common trait thoroughly documented, being regarded as a key probiotic antimicrobial strategy. Although some studies have pointed to the direct immunomodulatory effects of these bacteriocins in mammals, this has been largely unexplored in fish. To this aim, in the current study, we have investigated the immunomodulatory effects of bacteriocins, by comparing the effects of a wild type nisin Z-expressing Lactococcus cremoris strain of aquatic origin to those exerted by a non-bacteriocinogenic isogenic mutant and a recombinant nisin Z, garvicin A and Q-producer multi-bacteriocinogenic strain. The transcriptional response elicited by the different strains in the rainbow trout intestinal epithelial cell line (RTgutGC) and in splenic leukocytes showed significant differences. Yet the adherence capacity to RTgutGC was similar for all strains. In splenocyte cultures, we also determined the effects of the different strains on the proliferation and survival of IgM+ B cells. Finally, while the different LAB elicited respiratory burst activity similarly, the bacteriocinogenic strains showed an increased ability to induce the production of nitric oxide (NO). The results obtained reveal a superior capacity of the bacteriocinogenic strains to modulate different immune functions, pointing to a direct immunomodulatory role of the bacteriocins, mainly nisin Z.

Keywords: bacteriocins; fish; immunomodulation; lactic acid bacteria; nisin; probiotics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteriocins* / pharmacology
  • Lactobacillales*
  • Lactococcus lactis* / genetics
  • Lactococcus lactis* / metabolism
  • Mammals
  • Oncorhynchus mykiss* / microbiology

Substances

  • Bacteriocins

Supplementary concepts

  • Lactococcus lactis subsp. cremoris

Grants and funding

This work was supported by the Ministerio de Ciencia e Innovación (MICINN, Madrid, Spain) (projects RTI2018-094907-B-I00, and PID2020-113268RB-I00), and the Universidad Complutense de Madrid (UCM) (project FEI16/54). DC was supported by a contract from the project RTI2018-094907-B-I00. JF was supported by a FEI16/54 contract and held a predoctoral contract from UCM. LD-F was supported by a contract from the “Programa Investigo” (Ministerio de Trabajo y Economía Social, Madrid, Spain), funded by the EU (NextGenerationEU). JB was supported by the Atracción de Talento, program of the Comunidad de Madrid, Spain (2018-T1/BIO-10158).