Microbial dynamics and Pseudomonas natural product production in milk and dairy products

Abstract

Covering: 2000 up to the first half of 2024Milk and its derived dairy products have long been integral to the human diet, with evidence of consumption dating back over 9000 years. Milk's high nutritional value renders dairy products an important element of human diet while also offering a fertile environment for microbial growth. Beneficial microorganisms in dairy products are often associated with biogenic and probiotic effects, whereas spoilage or pathogenic microorganisms can pose health risks. Fermentation is a key method to preserve milk. Whereas dairying practices in most parts of the world have been highly altered by industrialization over the past century, nomadic pastoralists in Mongolia notably retain a rich tradition of household-level dairy fermentation that has been practiced since 3000 BC. Milk-associated microorganisms produce a vast number of low molecular weight natural products that can mediate beneficial and detrimental interactions. Bacteria of the genus Pseudomonas are found in traditional Mongolian dairy products and are common contaminants in commercial dairy products, and they can strongly impact the quality and shelf-life of dairy products. These bacteria are well known for their ability to produce a variety of secondary metabolites, including nonribosomal (lipo)peptides, which are both structurally and functionally diverse. Lipopeptides can have antimicrobial properties, act as quorum sensing molecules, and contribute to biofilm formation due to their amphiphilic nature. Although often associated with spoilage, some of these natural products can also exhibit positive effects with potential beneficial applications in the dairy industry. This review aims to provide a comprehensive overview of the interplay between culinary fermentation and the production and activities of microbial-derived natural products.

Fig. 1. Process of producing typical Mongolian dairy products.

Fig. 2. Overview of lactic acid bacteria (LAB) in raw milk. Created with BioRender.

Fig. 3. Complex interaction between lactic acid bacteria (LAB) and yeast in milk results in growth promotion and/or inhibition. Created with BioRender.

Fig. 4. Genetic organization of the most common classes of the aprX-lipA2 operon in Pseudomonas. Adapted from Maier et al. Created with BioRender.

Fig. 5. Example of chemical structures of six major classes of secondary metabolites from Pseudomonas. Polyketide (PK) mupirocin from P. fluorescens NCIMB 10586, nonribosomal peptide (NRP) pyoverdine from P. aeruginosa PAO, nonribosomal peptide/polyketide hybrid (NRP/PK hybrid) coronatine from P. syringae pv. glycinea PG4180, alkaloid safracin B from P. fluorescens A2-2, ribosomally synthesized and post-translationally modified peptide (RiPP) pseudomonassin from Pseudomonas sp. SST3, and terpene chlororaphen from P. chlororaphis O6.

Fig. 6. Family classification and chemical structures of short cyclic lipopeptides (CLPs) from pathogenic and non-pathogenic Pseudomonas strains. The characteristic combination of peptide length (L) and macrolactone ring size (S) is given in brackets after the family name as [L:S]. The individual member names from left to right: amphisin, viscosin, syringomycin E, bananamide A, orfamide A, poaeamide A, MA026, putisolvin I, ferrocin A, entolysin A, asplenin, and cocoyamide or gacamide A.

Fig. 7. Family classification and chemical structures of long cyclic lipopeptides (CLPs) from pathogenic and non-pathogenic Pseudomonas strains. The characteristic combination of peptide length (L) and macrolactone ring size (S) is given in brackets after the family name as [L:S]. The individual member names from left to right: tolaasin I, SP22-A, corpeptin A and fuscopeptin A.

Fig. 8. Family classification and chemical structures of linear lipopeptides (LLPs) from pathogenic and non-pathogenic Pseudomonas strains. The characteristic combination of peptide length (L) and macrolactone ring size (S) is given in brackets after the family name as [L:S]. The individual member names from left to right: syringafactin A, corrugatin, and thanafactin A.

Fig. 9. Overview of antagonistic activities, different functions, and applications of LPs. They exhibit a broad spectrum of antimicrobial activities including antibacterial, antifungal, anti-oomycete, antiprotozoal, antiviral, phytotoxic, herbicidal, and insecticidal activities. They promote bacterial mobility and are involved in surface attachment and biofilm formation. LPs play an important role in ecological interactions with plants or other organisms. Some LPs enhance the nutrient availability and degradation of toxic compounds and possess cytotoxic properties. It is beneficial in milk and dairy products that LPs have antioxidative and antiadhesive properties and can prevent biofilms. LPs inhibit the growth of pathogens in milk and favor the growth of beneficial microbes, while also enhancing the flavor and texture of dairy products. Due to their wide spectrum of activities and functions, LPs have many applications in the pharmaceutical and food industries. Created with BioRender.