Genome Sequences of Serratia Strains Revealed Common Genes in Both Serratomolides Gene Clusters

Abstract

Serratia strains are ubiquitous microorganisms with the ability to produce serratomolides, such as serrawettins. These extracellular lipopeptides are described as biocides against many bacteria and fungi and may have a nematicidal activity against phytopathogenic nematodes. Serrawettins W1 and W2 from different strains have different structures that might be correlated with distinct genomic organizations. This work used comparative genomics to determine the distribution and the organization of the serrawettins biosynthetic gene clusters in all the 84 publicly available genomes of the Serratia genus. The serrawettin W1 and W2 gene clusters' organization was established using antiSMASH software and compared with single and short data previously described for YD25^T Serratia. Here, the serrawettin W1 gene clusters' organization is reported for the first time. The serrawettin W1 biosynthetic gene swrW was present in 17 Serratia genomes. Eighty different coding sequence (CDS) were assigned to the W1 gene cluster, 13 being common to all clusters. The serrawettin W2 swrA gene was present in 11 Serratia genomes. The W2 gene clusters included 68 CDS with 24 present in all the clusters. The genomic analysis showed the swrA gene constitutes five modules, four with three domains and one with four domains, while the swrW gene constitutes one module with four domains. This work identified four genes common to all serrawettin gene clusters, highlighting their essential potential in the serrawettins biosynthetic process.

Keywords: Serratia; biosynthetic gene cluster; genome; serratomolides; serrawettin; swrA gene; swrW gene.

Figure 1

A phylogenetic dendrogram based on a comparison of the 16S rRNA gene sequence of the Serratia strains used in this study and the type of strains. The tree was created using the Neighbor-Joining method in ARB software. The numbers on the tree indicate the percentages of bootstrap sampling, derived from 1000 replications; values below 50% are not shown. In blue are shown the Serratia strains that showed the presence of the serrawettin W1 biosynthetic gene cluster and in green are shown the Serratia strains that showed the presence of the serrawettin W2 biosynthetic gene cluster. The type species Escherichia coli DSM 30083^T was used as the outgroup. Scale bar, 1 inferred nucleotide substitution per 100 nucleotides.

Figure 2

Serrawettin W1: from the biosynthetic gene cluster to the structure of serrawettin W1. Genetic organization of the genome of Serratia strain AS13 by antiSMASH analysis, Phyre2 tridimensional prediction of serrawettin W1 biosynthetic protein, and PubChem 2D structure of serrawettin W1. (a) Serrawettin W1 biosynthetic gene cluster with identification of the srwW core gene; (b) swrW gene organization: C, condensation domain; A, adenylation domain; T, thiolation domain; and TE, thioesterase domain; (c) biosynthetic protein with the condensation, adenylation, thiolation, and thioesterase domains; (d) serrawettin W1 2D structure.

Figure 3

Serrawettin W1 gene cluster analysis. The phylogenetic relationship was established with Mega X software by the Neighbor-Joining method on aligned serrawettin W1 gene clusters of Serratia strains ATCC 13880, CDC_813-60 DP21, UMH8, IOMTU 115, DSM 21420, VGH107, EGD-HP20, WW4, FS14, BIDMC81, TEL NODE_13, NBRC 102599, BXF1, A2, AS13, AS9, and AS12. (a) Phylogenetic tree based on protein sequences of the serrawettin W1 biosynthetic gene cluster on an established genetic organization. (b) Serrawettin W1 biosynthetic gene clusters based on natural genetic organization. (c) Comparison of the phylogenetic tree based on protein sequences of the serrawettin W1 biosynthetic gene clusters (left) with the phylogenetic tree of the serrawettin W1 biosynthesis protein (right). The scale bar of 0.050 infers the nucleotide substitutions per 100 nucleotides.

Figure 4

Serrawettin W2: from the biosynthetic gene cluster to the structure of serrawettin W2. Genetic organization of the genome of Serratia strain PWN146 by antiSMASH analysis, Phyre2 tridimensional prediction of the serrawettin W2 biosynthetic protein, and PubChem 2D structure of serrawettin W2. (a) Serrawettin W2 biosynthetic gene cluster with identification of the swrA core gene; (b) swrA gene organization: five modules (M1–M5) with C, condensation domain; A, adenylation domain; T, thiolation domain; and TE, thioesterase domain; (c) biosynthetic protein with five modules (M1–M5), each composed of condensation, adenylation, and thiolation domains, and in the last module an additional thioesterase domain.

Figure 5

Serrawettin W2 gene cluster analysis. The phylogenetic relationship was established with Mega X software by the Neighbor-Joining method on aligned serrawettin W1 gene clusters of Serratia strains PWN146, SSNIH1, SM39, SmUNAm836, BIDMC44, Lr5/4 LG59, RSC-14, AH0650, Db11, SCBI, and YD25^T. (a) Phylogenetic tree based on protein sequences of serrawettin W2 biosynthetic gene clusters on an established genetic organization. (b) Serrawettin W2 biosynthetic gene clusters based on natural genetic organization. (c) Comparison of the phylogenetic tree based on protein sequences of the serrawettin W1 biosynthetic gene clusters (left) with the phylogenetic tree of the serrawettin W1 biosynthesis protein (right). The scale bar of 0.050 infers nucleotide substitutions per 100 nucleotides.