A multifunctional polysaccharide utilization gene cluster in colwellia echini encodes enzymes for the complete degradation of κ-carrageenan, ι-carrageenan, and hybrid β/κ-carrageenan

Line Christiansen, Duleepa Pathiraja, Pernille Kjersgaard Bech, Mikkel Schultz-Johansen, Rosanna Hennessy, David Teze, In Geol Choi, Peter Stougaard

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)

Abstract

Algal cell wall polysaccharides constitute a large fraction in the biomass of marine primary producers and are thus important in nutrient transfer between trophic levels in the marine ecosystem. In order for this transfer to take place, polysaccharides must be degraded into smaller mono-and disaccharide units, which are subsequently metabolized, and key components in this degradation are bacterial enzymes. The marine bacterium Colwellia echini A3T is a potent enzyme producer since it completely hydrolyzes agar and-carrageenan. Here, we report that the genome of C. echini A3T harbors two large gene clusters for the degradation of carrageenan and agar, respectively. Phylogenetical and functional studies combined with transcriptomics and in silico structural modeling revealed that the carrageenolytic cluster encodes furcellaranases, a new class of glycoside hydrolase family 16 (GH16) enzymes that are key enzymes for hydrolysis of furcellaran, a hybrid carrageenan containing both-and-carrageenan motifs. We show that furcellaranases degrade furcellaran into neocarratetraose-43-O-monosulfate [DA-(α1,3)-G4S-(β1,4)-DA-(α1,3)-G], and we propose a molecular model of furcellaranases and compare the active site architectures of furcellaranases, κ-carrageenases, ι-agarases, and β-porphyranases. Furthermore, C. echini A3T was shown to encode κ-carrageenases, ι-carrageenases, and members of a new class of enzymes, active only on hybrid β/κ-carrageenan tetrasaccharides. On the basis of our genomic, transcriptomic, and functional analyses of the carrageenolytic enzyme repertoire, we propose a new model for how C. echini A3T degrades complex sulfated marine polysaccharides such as furcellaran, κ-carrageenan, and ι-carrageenan.

Original languageEnglish
Article number0792
Pages (from-to)1-16
Number of pages16
JournalmSphere
Volume5
Issue number1
DOIs
Publication statusPublished - 2020 Jan 1

Keywords

  • Algal polysaccharides
  • Carrageenan
  • Furcellaran
  • Glycoside hydrolases
  • Marine bacteria
  • Metabolic pathway

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

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