A Novel Auxiliary Agarolytic Pathway Expands Metabolic Versatility in the Agar-Degrading Marine Bacterium Colwellia echini A3T

Duleepa Pathiraja, Line Christiansen, Byeonghyeok Park, Mikkel Schultz-Johansen, Geul Bang, Peter Stougaard, In Geol Choi

Research output: Contribution to journalArticlepeer-review

16 Citations (Scopus)

Abstract

Marine microorganisms encode a complex repertoire of carbohydrate-active enzymes (CAZymes) for the catabolism of algal cell wall polysaccharides. While the core enzyme cascade for degrading agar is conserved across agarolytic marine bacteria, gain of novel metabolic functions can lead to the evolutionary expansion of the gene repertoire. Here, we describe how two less-abundant GH96 a-agarases harbored in the agar-specific polysaccharide utilization locus (PUL) of Colwellia echini strain A3T facilitate the versatility of the agarolytic pathway. The cellular and molecular functions of the a-agarases examined by genomic, transcriptomic, and biochemical analyses revealed that a-agarases of C. echini A3T create a novel auxiliary pathway. a-Agarases convert even-numbered neoagarooligosaccharides to odd-numbered agaroand neoagarooligosaccharides, providing an alternative route for the depolymerization process in the agarolytic pathway. Comparative genomic analysis of agarolytic bacteria implied that the agarolytic gene repertoire in marine bacteria has been diversified during evolution, while the essential core agarolytic gene set has been conserved. The expansion of the agarolytic gene repertoire and novel hydrolytic functions, including the elucidated molecular functionality of a-agarase, promote metabolic versatility by channeling agar metabolism through different routes. IMPORTANCE Colwellia echini A3T is an example of how the gain of gene(s) can lead to the evolutionary expansion of agar-specific polysaccharide utilization loci (PUL). C. echini A3T encodes two a-agarases in addition to the core b-agarolytic enzymes in its agarolytic PUL. Among the agar-degrading CAZymes identified so far, only a few a-agarases have been biochemically characterized. The molecular and biological functions of two a-agarases revealed that their unique hydrolytic pattern leads to the emergence of auxiliary agarolytic pathways. Through the combination of transcriptomic, genomic, and biochemical evidence, we elucidate the complete a-agarolytic pathway in C. echini A3T. The addition of a-agarases to the agarolytic enzyme repertoire might allow marine agarolytic bacteria to increase competitive abilities through metabolic versatility.

Original languageEnglish
Pages (from-to)1-19
Number of pages19
JournalApplied and environmental microbiology
Volume87
Issue number12
DOIs
Publication statusPublished - 2021 May

Bibliographical note

Funding Information:
This work was supported by a grant for bilateral collaboration between the National Research Foundation of Korea (2017K1A3A1A69086063), the Danish Agency for Science and Higher Education (7107-00014B), the Novo Nordisk Foundation (grant no. NNF12OC0000797), the Danish Council for Independent Research, Technology and Production Sciences (0602-02399B), New and Renewable Energy Core Technology Program of the Korea Institute of Energy Technology Evaluation and Planning (KETEP) grants from the Ministry of Trade, Industry and Energy (no. 20173010092460), and the School of Life Sciences and Biotechnology for BK21 PLUS, Korea University.

Publisher Copyright:
Copyright © 2021 American Society for Microbiology. All Rights Reserved.

Keywords

  • GH96
  • a-agarase
  • agar metabolism
  • agarase
  • gene gain
  • metabolic versatility
  • novel auxiliary pathway
  • polysaccharide utilization loci

ASJC Scopus subject areas

  • Biotechnology
  • Food Science
  • Ecology
  • Applied Microbiology and Biotechnology

Fingerprint

Dive into the research topics of 'A Novel Auxiliary Agarolytic Pathway Expands Metabolic Versatility in the Agar-Degrading Marine Bacterium Colwellia echini A3T'. Together they form a unique fingerprint.

Cite this