The planctomycete Stieleria maiorica Mal15T employs stieleriacines to alter the species composition in marine biofilms

Abstract

Bacterial strains of the phylum Planctomycetes occur ubiquitously, but are often found on surfaces of aquatic phototrophs, e.g. alga. Despite slower growth, planctomycetes are not outcompeted by faster-growing bacteria in biofilms on such surfaces; however, strategies allowing them to compensate for slower growth have not yet been investigated. Here, we identified stieleriacines, a class of N-acylated tyrosines produced by the novel planctomycete Stieleria maiorica Mal15T, and analysed their effects on growth of the producing strain and bacterial species likely co-occurring with strain Mal15T. Stieleriacines reduced the lag phase of Mal15T and either stimulated or inhibited biofilm formation of two bacterial competitors, indicating that Mal15T employs stieleriacines to specifically alter microbial biofilm composition. The genetic organisation of the putative stieleriacine biosynthetic cluster in strain Mal15T points towards a functional link of stieleriacine biosynthesis to exopolysaccharide-associated protein sorting and biofilm formation.

Stieleria varia sp. nov., isolated from wood particles in the Baltic Sea, constitutes a novel species in the family Pirellulaceae within the phylum Planctomycetes

“…Abbreviations: n.o. not observed Analysis of gene clusters putatively involved in the production of secondary metabolites Given the relatively large genomes of 9.6-11.0 Mb observed for the hitherto characterised species in the genus Stieleria, they are probably amongst the talented producers of secondary metabolites in the phylum Planctomycetes as confirmed by recently published studies (Kallscheuer et al 2020a;Sandargo et al 2020). We thus analysed the three genomes using antiSMASH to check for gene clusters potentially related to secondary metabolite production ( Table 3).…”

“…These numbers are in the upper range when considering the range of 1-13 clusters identified by antiSMASH in strains belonging to the phylum Planctomycetes (Wiegand et al 2020). S. neptunia Enr13 T and S. maiorica Mal15 T harbour N-acyl amino acid synthase-encoding genes, which are most likely involved in the biosynthesis of stieleriacines, a class of N-acylated tyrosine derivatives found to be produced by these two strains (Kallscheuer et al 2020a;Sandargo et al 2020) ( Table 3). However, in the still non-closed genome of strain Pla52n T we could not identify genes coding for putative N-acyl amino acid synthases, which might indicate that strain Pla52n T does not produce stieleriacines.…”

“…Maximum likelihood phylogenetic trees based on 16S rRNA genes sequences and MLSA place strain Pla52n T in the recently introduced family Pirellulaceae (Dedysh et al 2019). In this family, strain Pla52n T clusters monophyletically with two recently described species of the genus Stieleria, namely S. maiorica and S. neptunia (Kallscheuer et al 2020a;Sandargo et al 2020) (Fig. 1).…”

“…Maximum likelihood phylogeny was computed for strain Pla52n T , the type strains of all described planctomycetal species (assessed in May 2020) including strains of the family Pirellulaceae published and described in the recent year (Kallscheuer et al 2019a(Kallscheuer et al , c, 2020aKumar et al 2020;Peeters et al 2020a, b;Rensink et al 2020;Sandargo et al 2020). Phylogenetic trees based on 16S rRNA gene sequences and multi-locus sequence analysis (MLSA) were calculated as previously described (Boersma et al 2019).…”

“…Recently, a class of N-acylated tyrosine derivatives, designated stieleriacines, has been identified in the Planctomycete Stieleria maiorica Mal15 T , which can influence the microbial community composition of biofilms inhabited by this species (Kallscheuer et al 2020a). Structurally related compounds of the same class were also found in the closely related species Stieleria neptunia (Sandargo et al 2020).…”