Submerged and Solid-State Fermentation of Spirulina with Lactic Acid Bacteria Strains: Antimicrobial Properties and the Formation of Bioactive Compounds of Protein Origin

SIMPLE SUMMARY: Spirulina (Arthrospira platensis) is an edible blue-green alga that shows many desirable physiological activities in humans and animals. In this study, we hypothesized that the Spirulina composition can be improved (by increasing the gamma-aminobutyric acid concentration) during biotreatment with selected lactic acid bacteria (LAB) strains. Fermentation is the most popular and typically economically effective solution in the food and feed industry and used as biotechnology for the bioconversion of materials to higher-added-value products. However, in addition to desirable compounds, LAB are involved in the processes of biogenic amine formation. This study showed that most of the fermented Spirulina samples possess exceptional antimicrobial activity against Staphylococcus. However, the ratios of biogenic amine/gamma-aminobutyric acid and biogenic amine/L-glutamic acid ranged from 0.5 to 62 and from 0.31 to 10.7, respectively. It was concluded that the formation of non-desirable compounds (biogenic amines) must also be considered due to the similar mechanism of their synthesis as well as the possibility of obtaining high concentrations in the end products. ABSTRACT: The aim of this study was to investigate the changes in bioactive compounds (L-glutamic acid (L-Glu), gamma-aminobutyric acid (GABA) and biogenic amines (BAs)) during the submerged (SMF) and solid-state (SSF) fermentation of Spirulina with lactobacilli strains (Lacticaseibacillus paracasei No. 244; Levilactobacillus brevis No. 173; Leuconostoc mesenteroides No. 225; Liquorilactobacillus uvarum No. 245). The antimicrobial properties of the untreated and fermented Spirulina against a variety of pathogenic and opportunistic strains were tested. The highest concentrations of L-Glu (3841 mg/kg) and GABA (2396 mg/kg) were found after 48 h of SSF with No. 173 and No. 244 strains, respectively. The LAB strain used for biotreatment and the process conditions, as well as the interaction of these factors, had statistically significant effects on the GABA concentration in Spirulina (p ≤ 0.001, p = 0.019 and p = 0.011, respectively). In all cases, the SSF of Spirulina had a higher total BA content than SMF. Most of the fermented Spirulina showed exceptional antimicrobial activity against Staphylococcus aureus but not against the other pathogenic bacteria. The ratios of BA/GABA and BA/L-Glu ranged from 0.5 to 62 and from 0.31 to 10.7, respectively. The GABA content was correlated with putrescine, cadaverine, histamine, tyramine, spermidine and spermine contents. The L-glutamic acid concentration showed positive moderate correlations with tryptamine, putrescine, spermidine and spermine. To summarize, while high concentrations of desirable compounds are formed during fermentation, the formation of non-desirable compounds (BAs) must also be considered due to the similar mechanism of their synthesis as well as the possibility of obtaining high concentrations in the end products.