Abstract
Recently, we isolated two marine strains, F1T and F21T, which together with Kiritimatiella glycovorans L21-Fru-ABT are the only pure cultures of the class Kiritimatiellae within the phylum Verrucomicrobiota. Here, we present an in-depth genome-guided characterization of both isolates with emphasis on their exopolysaccharide synthesis. The strains only grew fermentatively on simple carbohydrates and sulfated polysaccharides. Strains F1T, F21T and K. glycovorans reduced elemental sulfur, ferric citrate and anthraquinone-2,6-disulfonate during anaerobic growth on sugars. Both strains produced exopolysaccharides during stationary phase, probably with intracellularly stored glycogen as energy and carbon source. Exopolysaccharides included N-sulfated polysaccharides probably containing hexosamines and thus resembling glycosaminoglycans. This implies that the isolates can both degrade and produce sulfated polysaccharides. Both strains encoded an unprecedently high number of glycoside hydrolase genes (422 and 388, respectively), including prevalent alpha-L-fucosidase genes, which may be necessary for degrading complex sulfated polysaccharides such as fucoidan. Strain F21T encoded three putative glycosaminoglycan sulfotransferases and a putative sulfate glycosaminoglycan biosynthesis gene cluster. Based on phylogenetic and chemotaxonomic analyses, we propose the taxa Pontiella desulfatans F1T gen. nov., sp. nov. and Pontiella sulfatireligans F21T sp. nov. as representatives of the Pontiellaceae fam. nov. within the class Kiritimatiellae.
Highlights
Unlike strain F21T cultures, cultures of strain F1T had a yellow color. This may be due to the formation of lycopene, other carotenoids and/or aryl polyenes, as genes involved in their synthesis were encoded in the genome of strain F1T but not in that of strain F21T
The ability of strains F1T and F21T to grow on different types of fucoidan is consistent with the expansive carbohydrate-active enzymes (CAZymes) gene repertoires presented here and the reported sulfatase gene repertoires [8]
It should be noted that the degradation of fucoidan by bacteria has been shown to involve fucosidases [60], fucoidanases [61,62,63], deacetylases [64] and sulfatases [65], there is currently no model of the exact enzymatic mechanism by which bacteria break down fucoidan into monomers
Summary
Sulfated polysaccharides are prevalent in marine environments, where they are produced in high quantities by macroalgae, microalgae and bacteria [3]. This class of compounds forms an important substrate for marine microorganisms due to their prevalence. Degradation of sulfated polysaccharides involves the removal of sulfate groups by sulfatases [4]. Sulfatase genes are present in high numbers in the genomes of some marine bacteria of the Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) superphylum such as Rhodopirellula baltica SH1T [5] and Lentisphaera araneosa HTCC2155T [6], supporting the idea that PVC bacteria are likely to be key degraders of sulfated polysaccharides in the marine environment. Anaerobic strains of sulfatase-rich PVC bacteria have rarely been studied far, despite the importance of anoxic marine sediments in the mineralization process [7]
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