Ratio of Histamine-Producing/Non-Histamine-Producing Subgroups of Tetragenococcus halophilus Determines the Histamine Accumulation during Spontaneous Fermentation of Soy Sauce.

Abstract

Strain specificity (within-species variation) of microorganisms occurs widely in nature. It might affect microbiome construction and function in a complex microbial environment. Tetragenococcus halophilus, a halophilic bacterium that generally is used in high salt food fermentation, consists of two histamine-producing and non-histamine-producing subgroups. It is unclear whether and how the strain specificity of histamine-producing capacity influences the microbial community function during food fermentation. Here, based on systematic bioinformatic analysis, histamine production dynamic analysis, clone library construction analysis, and cultivation-based identification, we identified that T. halophilus is the focal histamine-producing microorganism during soy sauce fermentation. Furthermore, we discovered that a larger number and ratio of histamine-producing subgroups of T. halophilus significantly contributed more histamine production. We were able to artificially decrease the ratio of histamine-producing to non-histamine-producing subgroups of T. halophilus in complex soy sauce microbiota and realized the reduction of histamine by 34%. This study emphasizes the significance of strain specificity in regulating microbiome function. This study investigated how strain specificity influenced microbial community function and developed an efficient technique for histamine control. IMPORTANCE Inhibiting the production of microbiological hazards under the assumption of stable and high-quality fermentation is a critical and time-consuming task for the food fermentation industry. For spontaneously fermented food, it can be realized theoretically by finding and controlling the focal hazard-producing microorganism in complex microbiota. This work used histamine control in soy sauce as a model and developed a system-level approach to identify and regulate the focal hazard-producing microorganism. We discovered that the strain specificity of focal hazard-producing microorganisms had an important impact on hazard accumulation. Microorganisms frequently exhibit strain specificity. Strain specificity is receiving increasing interest since it determines not only microbial robustness but also microbial community assembly and microbiome function. This study creatively explored how the strain specificity of microorganisms influenced microbiome function. In addition, we believe that this work provides an excellent model for microbiological hazard control which can promote future work in other systems.