Stieleria sedimenti sp. nov., a Novel Member of the Family Pirellulaceae with Antimicrobial Activity Isolated in Portugal from Brackish Sediments

Abstract

The phylum Planctomycetota is known for having uncommon biological features. Recently, biotechnological applications of its members have started to be explored, namely in the genus Stieleria. Here, we formally describe a novel Stieleria isolate designated as strain ICT_E10.1T, obtained from sediments collected in the Tagus estuary (Portugal). Strain ICT_E10.1T is pink-pigmented, spherical to ovoid in shape, and 1.7 µm ± 0.3 × 1.4 µm ± 0.3 in size. Cells cluster strongly in aggregates or small chains, divide by budding, and have prominent fimbriae. Strain ICT_E10.1T is heterotrophic and aerobic. Growth occurs from 20 to 30 °C, from 0.5 to 3% (w/v) NaCl, and from pH 6.5 to 11.0. The analysis of the 16S rRNA gene sequence placed strain ICT_E10.1T into the genus Stieleria with Stieleria neptunia Enr13T as the closest validly described relative. The genome size is 9,813,311 bp and the DNA G+C content is 58.8 mol%. Morphological, physiological, and genomic analyses support the separation of this strain into a novel species, for which we propose the name Stieleria sedimenti represented by strain ICT_E10.1T as the type of strain (=CECT 30514T= DSM 113784T). Furthermore, this isolate showed biotechnological potential by displaying relevant biosynthetic gene clusters and potent activity against Staphylococcus aureus.

Uncovering the biotechnological capacity of marine and brackish water Planctomycetota

“…The biological material analyzed in this study included twenty-three planctomycetal strains belonging to our culture collection (Laboratory for Microbial Ecophysiology of the University of Porto, Portugal-LEMUP). These strains were previously isolated from different samples collected in marine and estuarine environments in various regions of Portugal (Bondoso, et al , 2015Godinho et al 2021;Lage and Bondoso 2011;Vitorino, et al 2020Vitorino, et al , 2021bVitorino, et al , 2022bVitorino, et al , 2022cVitorino, et al , 2023Vitorino, et al , 2022d. They are all affiliated to the class Planctomycetia within the phylum Planctomycetota.…”

“…Coloured branches were used to differentiate each family: green for Lacipirellulaceae, orange for Pirellulaceae and blue for Planctomycetaceae. *data on the antibacterial effects of strain ICT_E10.1 T were taken from previous study (Vitorino, et al 2022b) for the production of bioactive molecules by these strains. Particularly, the extract of R. margarita ICM_H10 T inhibited the growth of all Enterococcus spp.…”

“…The vast majority of estimated bacterial diversity is still uncultured in laboratory (Barer and Harwood 1999;Rinke, et al 2013), which heavily restricts what could be screened for biotechnological purposes. Nonetheless, recent cultivation efforts from diverse research groups have allowed to bring into axenic culture many strains (including novel species) from underexplored and evolutionarily deep-branching groups such as the Planctomycetota (Almeida, et al 2022, Gaurav, et al 2021, Kaushik, et al 2020, Kulichevskaya, et al 2020a, Kulichevskaya, et al 2022, Kulichevskaya, et al 2020b, Kumar, et al 2020a, Kumar, et al 2020b, Kumar, et al 2021a, Vitorino, et al 2020, Vitorino et al 2021b, Vitorino, et al 2022b, Vitorino, et al 2022c, Vitorino, et al 2022d. The bacterial phylum Planctomycetes (now renamed Planctomycetota (Oren and Garrity 2021)) belongs to the super phylum Planctomycetota-Chlamydiota-Verrucomicrobiota (PVC) (Rivas-Marín and Devos 2018;Wagner and Horn 2006).…”

“…Most Planctomycetota have large genomes with many genes of unknown function and a comparatively high number of genes coding large proteins (Faria, et al 2018;Lage and Bondoso 2014;Wiegand, et al 2018), features that are shared with other well-known producers of bioactive compounds. Genome mining in many strains also demonstrated their rich content of putatively new biosynthetic gene clusters (BGCs) from several structural types (such as nonribosomal peptide synthases (NRPS) polyketide synthases (PKS), ribosomally synthesized and post-translationally modified peptides (RiPPs), lanthipeptides and bacteriocins), which are often linked to the production of bioactive secondary metabolites (Belova, et al 2020;Graca, et al 2016;Jeske, et al 2013;Kallscheuer and Jogler 2021;Vitorino, et al 2022bVitorino, et al , 2022d. Additionally, the capability of some Planctomycetota to produce antimicrobial and cytotoxic molecules was already confirmed through in vitro bioactivity screenings, including the description of the first (and the only one up to date) antimicrobial compounds from planctomycetal origin (Belova, et al 2020;Calisto, et al 2019;Graca, et al 2016;Jeske, et al 2016;Kallscheuer, et al 2020;).…”

“…1. Novel recently described species (Godinho et al 2021;Vitorino, et al 2020Vitorino, et al , 2021aVitorino, et al , 2022aVitorino, et al , 2022bVitorino, et al , 2022cVitorino, et al , 2023 were also included in this study. Metabolites from Planctomycetota cultured in oligotrophic medium were extracted with organic solvents and followed by antimicrobial and antifungal assays, in a first stage, against two different types of bacteria (the Gram-negative Escherichia coli and the Gram-positive Staphylococcus aureus) and three different fungi (the yeast Candida albicans and the filamentous fungi Trichophyton rubrum and Aspergillus fumigatus).…”