Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from black sea sediment

Daan M. van Vliet, Susakul Palakawong Na Ayudthaya, Sally Diop, Laura Villanueva, Alfons J.M. Stams, Irene Sánchez-Andrea

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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.

Original languageEnglish
Article number253
JournalFrontiers in Microbiology
Volume10
DOIs
Publication statusPublished - 18 Feb 2019

Fingerprint

Black Sea
Sulfatases
Polysaccharides
Carrageenan
Verrucomicrobia
Chlamydia
Bacteria
Sulfates
Hydrolysis
Water
Disaccharides
Enzymes
Post Translational Protein Processing
rRNA Genes
Genes
Minerals

Keywords

  • Desulfation
  • Kiritimatiellaeota
  • Marine
  • Novel anaerobes
  • Polysaccharide
  • Saccharolytic
  • Sulfatase

Cite this

@article{692e3ad407074539a73f7873c4005a5b,
title = "Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from black sea sediment",
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.",
keywords = "Desulfation, Kiritimatiellaeota, Marine, Novel anaerobes, Polysaccharide, Saccharolytic, Sulfatase",
author = "{van Vliet}, {Daan M.} and Ayudthaya, {Susakul Palakawong Na} and Sally Diop and Laura Villanueva and Stams, {Alfons J.M.} and Irene S{\'a}nchez-Andrea",
year = "2019",
month = "2",
day = "18",
doi = "10.3389/fmicb.2019.00253",
language = "English",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers",

}

Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from black sea sediment. / van Vliet, Daan M.; Ayudthaya, Susakul Palakawong Na; Diop, Sally; Villanueva, Laura; Stams, Alfons J.M.; Sánchez-Andrea, Irene.

In: Frontiers in Microbiology, Vol. 10, 253, 18.02.2019.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from black sea sediment

AU - van Vliet, Daan M.

AU - Ayudthaya, Susakul Palakawong Na

AU - Diop, Sally

AU - Villanueva, Laura

AU - Stams, Alfons J.M.

AU - Sánchez-Andrea, Irene

PY - 2019/2/18

Y1 - 2019/2/18

N2 - 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.

AB - 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.

KW - Desulfation

KW - Kiritimatiellaeota

KW - Marine

KW - Novel anaerobes

KW - Polysaccharide

KW - Saccharolytic

KW - Sulfatase

U2 - 10.3389/fmicb.2019.00253

DO - 10.3389/fmicb.2019.00253

M3 - Article

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 253

ER -