Genomic and gene expression evidence of nonribosomal peptide and polyketide production among ruminal bacteria: a potential role in niche colonization?

Abstract

Genomic and transcriptomic analyses were performed to investigate nonribosomal peptide synthetases (NRPS) and polyketide synthases (PKS) in 310 genomes of ruminal/fecal microorganisms. A total of 119 biosynthetic genes potentially encoding distinct nonribosomal peptides (NRPs) and polyketides (PKs) were predicted in the ruminal microbial genomes and functional annotation separated these genes into 19 functional categories. The phylogenetic reconstruction of the 16S rRNA sequences coupled to the distribution of the three ‘backbone’ genes involved in NRPS and PKS biosyntheses suggested that these genes were not acquired through horizontal gene transfer. Metatranscriptomic analyses revealed that the predominant genes involved in the synthesis of NRPs and PKs were more abundant in sheep rumen datasets. Reads mapping to the NRPS and PKS biosynthetic genes were represented in the active ruminal microbial community, with transcripts being highly expressed in the bacterial community attached to perennial ryegrass, and following the main changes occurring between primary and secondary colonization of the forage incubated with ruminal fluid. This study is the first comprehensive characterization demonstrating the rich genetic capacity for NRPS and PKS biosyntheses within rumen bacterial genomes, which highlights the potential functional roles of secondary metabolites in the rumen ecosystem.

In silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides

“…The genes considered essential to lasso peptide biosynthesis showed a low level of expression in the ruminal metatranscriptome datasets and were more expressed within the microbial community of the sheep rumen, which is in agreement with our previous observations indicating that non-ribosomal peptide synthetases (NRPS) and polyketide synthases (PKS) were also more abundant in the rumen microbiota of sheep (Moreira et al, 2020). Additionally, the reads corresponding to the genes found in Butyrivibrio sp., Lachnospira sp., and Ruminococcus sp.…”

“…Additionally, the reads corresponding to the genes found in Butyrivibrio sp., Lachnospira sp., and Ruminococcus sp. were most represented in the sheep metatranscriptomes, also confirming previous observations showing a higher prevalence of NRPS and PKS within members of these ruminal taxa (Moreira et al, 2020). Taken together, these results demonstrate the potential production of antimicrobial compounds by species of bacteria colonizing the rumen of sheep, which deserves further investigation.…”

“…The discovery of new lasso peptides may be hindered by the great sequence variation of these molecules. Previously, we applied genome mining approaches to explore the ruminal environment as a potential source of bacteriocins (Azevedo et al, 2015), and non-ribosomal peptides and polyketides (Moreira et al, 2020). Here, we performed an extensive in silico screen in publically available genomes of ruminal bacteria in an attempt to determine the prevalence and diversity of lasso peptides among major species of bacteria from the rumen.…”

“…In addition, two g ene clusters of sactipeptides and one cluster of a class III bacteriocin were found in Ruminococcus albus 8 ( Azevedo et al, 2015 ). Bacteriocin gene clusters were also identified in the genomes of Butyrivibrio fibrisolvens MD2001, Butyrivibrio proteoclasticus B316, Butyrivibrio proteoclasticus FD2007, and Lachnospira multipara MC2003 ( Azevedo et al, 2015 ), while genes associated with the biosynthesis of non-ribosomal peptides (NRP) and polyketides (PK) were reported in the genomes of Bacillus cereus KPR-7A and Clostridium beijerinckii HUN142 ( Moreira et al, 2020 ). Altogether, the presence of gene clusters encoding for distinct classes of antimicrobial compounds in ruminal bacteria suggest the importance of these molecules in the rumen ecosystem and highlight their potential applications in controlling undesirable bacteria.…”

Microbiomes attached to fresh perennial ryegrass- are temporally resilient and adapt to changing ecological niches

“…In contrast, we showed that expression of non-ribosomally synthesised peptides and polyketide increased during secondary colonisation within fresh PRG attached bacteria [81]. The DE of these ribosomally and non-ribosomally synthesised AMPs and polyketides during the transition from primary to secondary colonisation may well contribute towards the antagonism between the bacteria characteristic of the two phases of PRG colonisation.…”