Microbiome composition modulates secondary metabolism in a multispecies bacterial community

Abstract

Bacterial secondary metabolites are a major source of antibiotics and other bioactive compounds. In microbial communities, these molecules can mediate interspecies interactions and responses to environmental change. Despite the importance of secondary metabolites in human health and microbial ecology, little is known about their roles and regulation in the context of multispecies communities. In a simplified model of the rhizosphere composed of Bacillus cereus , Flavobacterium johnsoniae , and Pseudomonas koreensis , we show that the dynamics of secondary metabolism depend on community species composition and interspecies interactions. Comparative metatranscriptomics and metametabolomics reveal that the abundance of transcripts of biosynthetic gene clusters (BGCs) and metabolomic molecular features differ between monocultures or dual cultures and a tripartite community. In both two- and three-member cocultures, P. koreensis modified expression of BGCs for zwittermicin, petrobactin, and other secondary metabolites in B. cereus and F. johnsoniae, whereas the BGC transcriptional response to the community in P. koreensis itself was minimal. Pairwise and tripartite cocultures with P. koreensis displayed unique molecular features that appear to be derivatives of lokisin, suggesting metabolic handoffs between species. Deleting the BGC for koreenceine, another P. koreensis metabolite, altered transcript and metabolite profiles across the community, including substantial up-regulation of the petrobactin and bacillibactin BGCs in B. cereus , suggesting that koreenceine represses siderophore production. Results from this model community show that bacterial BGC expression and chemical output depend on the identity and biosynthetic capacity of coculture partners, suggesting community composition and microbiome interactions may shape the regulation of secondary metabolism in nature.

Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum

“…In agreement with other studies (Chevrette et al, 2022), RNA-Seq analysis revealed that the two microorganisms perceived the presence of each other in the in vitro co-culture (3 days after the co-inoculation), as evidenced by the reprogramming of both transcriptomes, compared to the single cultures. It could be argued that the transcriptome changes of AtB-42 (887 DEGs out of 2613 genes) were the result of the growth inhibition due to the presence of M10.…”

Enhancing chemical and biological diversity by co-cultivation

“…However, studies of microbial co-culture have achieved the use of more than two microorganisms in one culture system. Indeed, Chevrette and co-workers have discovered that the abundance of transcripts of BGCs and the metabolic profiles differ between monocultures, dual-cultivation, and a tripartite community and that the dynamics of specialized metabolism depend on the interspecies interactions and the community species composition ( Chevrette et al, 2022 ). To exemplify these dynamics, Pettit and co-workers have simultaneously co-cultured five fungi ( Ovadendron sulphureoochraceum , Ascochyta pisi , Emericellopsis minima , Cylindrocarpon destructans , and Fusarium oxysporum ) for the biosynthesis of potential antineoplastic substances.…”

Metagenomics Reveals the Microbiome Multifunctionalities of Environmental Importance From Termite Mound Soils

“…7 The dominance of Proteobacteria and Actinobacteria in termite mound soils from this study supported this fact as some strains ( Bacillus, Pseudomonas and Streptomyces species) from Proteobacteria and Actinobacteria are recognized to synthesize almost 80% of the total metabolites identified nowadays. 30,31 It has also been established that well-known antimicrobial compounds like streptothricin, actinomycin, and streptomycin, which are of agricultural significance, are produced by some species of the Actinobacteria , 32 which was very abundant in termite mound soils from this study.…”

“…33 Our study revealed a lot of pathways and genes that code for secondary metabolism (Figure 3 and Supplemental Table S3), a unique characteristic of microorganisms to synthesize a variety of metabolites that are significant for self-defense. 32 They also play huge function in microbe–microbe, host–microbe, and microbe–environment collaborations. 34 The presence of genes linked to auxin biosynthesis (a growth regulator influencing the cell elongation and division in plants) in our study shows that termite mound soil housed auxin-producing and auxin-secreting microbiome.…”