Reduction of biogenic amines formation during soybean paste fermentation by using Staphylococcus carnosus M43 and Pediococcus acidilactici M28 as starter culture

Highlights

• Pediococcus acidilactici M28 was able to degrade all eight kinds of BAs.

• Staphylococcus carnosus M43 showed strong ability to degrade HIS and TYR.

• Application of two strains significantly reduced BAs formation during fermentation.

• These two strains produced more desirable flavor compounds during fermentation.

Abstract

Biogenic amines (BAs) are frequently presented in traditionally fermented food and can be controlled by biological methods. In this study, Pediococcus acidilactici M28 and Staphylococcus carnosus M43 with strong biogenic amines degrading ability were isolated from Chinese soybean paste. P. acidilactici M28 was able to degrade all eight kinds of biogenic amines while S. carnosus M43 could degrade high level of histamine and tyramine which were most commonly found and toxic in fermented food. The optimal histamine-tyramine degrading activity of P. acidilactici M28 and S. carnosus M43 were observed at pH5-7, 0–9% (w/v) NaCl and 30–40 °C. The application of P. acidilactici M28 and S. carnosus M43 as starter in lab-scale soybean paste fermentation not only reduced the BAs formation during fermentation but also produced more desirable flavor compounds. This study suggested that the use of P. acidilactici M28 and S. carnosus M43 as starter in soybean paste fermentation might be a good strategy for reduction of BAs formation.

Introduction

Biogenic amines (BAs) are a class of nitrogenous organic compounds and can be found in most of the fermented food, such as soy sauce, soybean paste, sausage, fish sauce, cheese, etc. BAs are generally synthesized via the microbial activities through decarboxylation of precursor amino acids. For example, cadaverine (CAD), tryptamine (TRY), phenethylamine (PHE), histamine (HIS) and tyramine (TYR) are produced by the corresponding precursor amino acids lysine, tryptophan, phenylalanine, histidine and tyrosine, respectively, through amino acids decarboxylase (K. H. Kim, Lee, Chun, Jeong, & Jeon, 2019). The excessive intake of BAs by human may cause severe health problems, such as headaches, hyper/hypotension, nausea, hot flushes, localized inflammation, heart palpitations and respiratory distress, especially in people who have reduced amine oxidase activity (Al Bulushi, Poole, Deeth, & Dykes, 2009; Anderson, Hasan, & McCrodden, 1993; Shalaby, 1996). Therefore, the level of BAs in food should be strictly controlled to ensure food safety.

Bean-based fermented food, such as tofu, soy sauce, sufu, doubanjiang (broad bean paste), natto, soymilk, soy sprouts, tempeh, miso, tamari and soybean paste, is popular in Europe, America and Asia due to its special flavor and rich nutrition (Papageorgiou et al., 2018). Beans are abundant in proteins, which would be degraded into amino acids through the activities of the multi-microbe system during fermentation and this might lead to the high risk of excessive BAs in bean-based fermented food. For example, the mean values of biogenic amines (PUT, CAD, SPD, SPM, TRY, PHE, HIS and TYR) in 23 doenjang samples were 708.4, 342.4, 744.1, 2443.6, 183.7, 820.3, 267.9 and 1266.6 mg/kg, respectively (Shukla, Park, Kim, & Kim, 2010). There are clear limits on HIS concentration in fish products (Commission Regulation (EC) 2073/2005) while FDA specifies the total BAs concentration in aquatic products is no more than 1000 mg/kg. However, the legislation concerning the concentrations of specific BAs in different kinds of food is still lacking. It was suggested that the upper limits of BAs in food is 100 mg of HIS per kg or 2 mg of HIS per liter of alcoholic beverage (Ten Brink, Damink, Joosten, & Huis in 't Veld, 1990). The overdose of BAs can cause negative physiological effects. Therefore, the high risk of BAs in bean-based fermented food attracts great attention from manufacturers and researchers.

Several methods have been proposed to control the BAs level in bean-based fermented food, such as irradiation (J.-H. Kim, Kim, Ahn, Park, & Byun, 2005), modified atmosphere packaging (Ruiz-Capillas, Pintado, & Jiménez-Colmenero, 2011), high hydrostatic pressure (Novella-Rodríguez, Veciana-Nogués, Saldo, & Vidal-Carou, 2003) and the addition of food additives and preservatives (Mah & Hwang, 2009; Naila, Flint, Fletcher, Bremer, & Meerdink, 2010). The addition of food additives and preservatives is efficient in inhibiting the growth of BAs-producing bacteria. However, food additives and preservatives have potential health hazardous for people. Therefore, biological methods, such as the inoculation of BAs degrading microbes, are preferred in recent years due to their safety for human and environment (Eom, Seo, & Choi, 2015; Kang, Kim, Mah, Kim, & Hwang, 2018). The histamine and total biogenic amine contents in Miso were reduced by 58% and 27%, respectively, when using the Lactobacillus plantarum D-103 strain as starter culture (Y. C. Lee et al., 2016). The co-inoculation of L. plantarum and Staphylococcus xylosus in Chinese rice wine led to a significant reduction of total BAs concentration (43.7%) (Xia, Luo, Zhang, Huang, & Zhang, 2018). Repressing of BAs formation during saeu-jeot (salted shrimp) fermentation was achieved using Tetragenococcus halophilus MJ4 with no-BA producing genes as starter culture (K. H. Kim et al., 2019). These biological methods have also been successfully applied in other kinds of fermented food, such as Cheonggukjang (Su-Yeon, Hyeong-Eun, & Yong-Suk, 2017), Doenjang (Shukla et al., 2015), doubanjiang (Byun, Bai, & Mah, 2013) and Chunjang (Bai, Byun, & Mah, 2013).

Soybean paste is a typical soybean-based fermented food in China and it is made using soybean as raw materials through fermentation by a variety of microbes (Jia et al., 2018). High level of BAs, especially HIS and TYR, were detected in soybean paste and their concentration increased during fermentation (Jia et al., 2018). Therefore, control of the BAs concentration during soybean paste fermentation is crucial for soybean paste industry. In this study, two bacteria strains with strong ability to degrade BAs were isolated from soybean paste and the effect of environmental factors, such as salt concentration, temperature and pH, on their ability to degrade BAs (especially HIS and TYR) was studied. These two strains were also applied in lab-scale soybean paste fermentation.