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

doi:10.1128/AEM.00230-21

A Novel Auxiliary Agarolytic Pathway Expands Metabolic Versatility in the Agar-Degrading Marine Bacterium Colwellia echini A3^T

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

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

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.

Originalsprog	Engelsk
Tidsskrift	Applied and Environmental Microbiology
Vol/bind	87
Nummer	12
Sider (fra-til)	1-19
Antal sider	19
ISSN	0099-2240
DOI	https://doi.org/10.1128/AEM.00230-21
Status	Udgivet - maj 2021
Udgivet eksternt	Ja

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10.1128/AEM.00230-21

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Citationsformater

@article{843dfed204d240168812cf34d09a0c14,

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

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.",

keywords = "a-agarase, agar metabolism, agarase, gene gain, GH96, metabolic versatility, novel auxiliary pathway, polysaccharide utilization loci",

author = "Duleepa Pathiraja and Line Christiansen and Byeonghyeok Park and Mikkel Schultz-Johansen and Geul Bang and Peter Stougaard and Choi, {In Geol}",

year = "2021",

month = may,

doi = "10.1128/AEM.00230-21",

language = "English",

volume = "87",

pages = "1--19",

journal = "Applied and Environmental Microbiology",

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publisher = "American Society for Microbiology",

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A Novel Auxiliary Agarolytic Pathway Expands Metabolic Versatility in the Agar-Degrading Marine Bacterium Colwellia echini A3^T. / Pathiraja, Duleepa; Christiansen, Line; Park, Byeonghyeok et al.
I: Applied and Environmental Microbiology, Bind 87, Nr. 12, 05.2021, s. 1-19.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

TY - JOUR

T1 - A Novel Auxiliary Agarolytic Pathway Expands Metabolic Versatility in the Agar-Degrading Marine Bacterium Colwellia echini A3T

AU - Pathiraja, Duleepa

AU - Christiansen, Line

AU - Park, Byeonghyeok

AU - Schultz-Johansen, Mikkel

AU - Bang, Geul

AU - Stougaard, Peter

AU - Choi, In Geol

PY - 2021/5

Y1 - 2021/5

N2 - 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.

AB - 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.

KW - a-agarase

KW - agar metabolism

KW - agarase

KW - gene gain

KW - GH96

KW - metabolic versatility

KW - novel auxiliary pathway

KW - polysaccharide utilization loci

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U2 - 10.1128/AEM.00230-21

DO - 10.1128/AEM.00230-21

M3 - Journal article

C2 - 33811026

AN - SCOPUS:85107090377

SN - 0099-2240

VL - 87

SP - 1

EP - 19

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

IS - 12

ER -