Abstract
The marine environment contains a large diversity of sulfated polysaccharides and other glycopolymers. Saccharolytic microorganisms degrade these compounds through hydrolysis, which includes the hydrolysis of sulfate groups from sugars by sulfatases. Various marine bacteria of the Planctomycetes-Verrucomicrobia-Chlamydia (PVC) superphylum have exceptionally high numbers of sulfatase genes associated with the degradation of sulfated polysaccharides. However, thus far no sulfatase-rich marine anaerobes are known. In this study, we aimed to isolate marine anaerobes using sulfated polysaccharides as substrate. Anoxic enrichment cultures were set up with a mineral brackish marine medium, inoculated with anoxic Black Sea sediment sampled at 2,100 m water depth water and incubated at 15°C (in situ T = 8°C) for several weeks. Community analysis by 16S rRNA gene amplicon sequencing revealed the enrichment of Kiritimatiellaeota clade R76-B128 bacteria in the enrichments with the sulfated polysaccharides fucoidan and iota-carrageenan as substrate. We isolated two strains, F1 and F21, which represent a novel family within the order of the Kiritimatiellales. They were capable of growth on various mono-, di-, and polysaccharides, including fucoidan. The desulfation of iota-carrageenan by strain F21 was confirmed quantitatively by an increase in free sulfate concentration. Strains F1 and F21 represent the first marine sulfatase-rich anaerobes, encoding more sulfatases (521 and 480, 8.0 and 8.4% of all coding sequences, respectively) than any other microorganism currently known. Specific encoded sulfatase subfamilies could be involved in desulfating fucoidan (S1_15, S1_17 and S1_25) and iota-carrageenan (S1_19). Strains F1 and F21 had a sulfatase gene classification profile more similar to aerobic than anaerobic sulfatase-rich PVC bacteria, including Kiritimatiella glycovorans, the only other cultured representative within the Kiritimatiellaeota. Both strains encoded a single anaerobic sulfatase-maturating enzyme which could be responsible for post-translational modification of formylglycine-dependent sulfatases. Strains F1 and F21 are potential anaerobic platforms for future studies on sulfatases and their maturation enzymes.
Highlights
Polysaccharides present a diversity of functions in different fields of biology
The degradation of fucoidan in enrichment cultures was apparent through the formation of transient degradation products hydrogen, acetate and propionate (Figure 1)
Strains F1 and F21 showed to be capable of growth of sulfated polysaccharides
Summary
Polysaccharides present a diversity of functions in different fields of biology. They have a structural role in cell walls of plants (e.g., cellulose and xylan) and fungi (e.g., chitin), as well as in the exoskeleton of arthropods which consist of chitin. Polysaccharides are the main constituent of peptidoglycan and lipopolysaccharides, which form the cell wall of most prokaryotes. Various polysaccharides (e.g., glycogen, starch, laminarin) are stored as energy reserve by animals, plants and microorganisms. Extracellular polysaccharides (exopolysaccharides) are the main constituent of extracellular polymeric substances (EPS; More et al, 2014). Microorganisms excrete EPS to facilitate attachment, aggregation and protection against grazing, desiccation or other stress factors (Wingender et al, 1999)
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