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Cite: NAR/gkaa742 2020



PUL General Information

Literature Information

PUL ID

PUL0652

PubMed

33811026, Appl Environ Microbiol. 2021 May 26;87(12):e0023021. doi: 10.1128/AEM.00230-21. Epub 2021 May 26.

Characterization method

RNA-Seq,enzyme activity assay,thin layer chromatography,liquid chromatography,mass spectrometry

Genomic accession number

NZ_PJAI02000001.1

Nucelotide position range

312864-408665

Substrate

agar

Loci

CWS31_RS01305-CWS31_RS01575

Species

Colwellia echini A3/1982103

Degradation or Biosynthesis

degradation

Gene Name

Locus Tag

Protein ID

Gene Position

GenBank Contig Range

EC Number

- CWS31_RS01305 WP_246143262.1 0 - 2574 (+) NZ_PJAI02000001.1:312864-315438 -
- CWS31_RS01310 WP_148747638.1 2662 - 4225 (+) NZ_PJAI02000001.1:315526-317089 -
- CWS31_RS01315 WP_148747639.1 4453 - 6742 (+) NZ_PJAI02000001.1:317317-319606 -
fdhD CWS31_RS01320 WP_148747640.1 6922 - 7663 (+) NZ_PJAI02000001.1:319786-320527 -
- CWS31_RS01325 WP_148747641.1 7962 - 10251 (+) NZ_PJAI02000001.1:320826-323115 -
- CWS31_RS01330 WP_148747642.1 10326 - 11004 (+) NZ_PJAI02000001.1:323190-323868 -
- CWS31_RS17905 WP_148747643.1 11704 - 15667 (+) NZ_PJAI02000001.1:324568-328531 -
- CWS31_RS17805 - 16403 - 17006 (+) NZ_PJAI02000001.1:329267-329870 -
- CWS31_RS01345 WP_148747645.1 19928 - 21002 (-) NZ_PJAI02000001.1:332792-333866 -
- CWS31_RS01350 WP_148747646.1 21137 - 21899 (-) NZ_PJAI02000001.1:334001-334763 -
- CWS31_RS01355 WP_148747647.1 22165 - 23785 (-) NZ_PJAI02000001.1:335029-336649 -
- CWS31_RS01360 WP_246143264.1 24325 - 26698 (+) NZ_PJAI02000001.1:337189-339562 -
- CWS31_RS01365 WP_246143290.1 26741 - 29012 (+) NZ_PJAI02000001.1:339605-341876 3.2.1.23
- CWS31_RS01370 WP_148747649.1 29130 - 30843 (+) NZ_PJAI02000001.1:341994-343707 -
- CWS31_RS01375 WP_170252732.1 31298 - 33680 (+) NZ_PJAI02000001.1:344162-346544 -
- CWS31_RS01380 WP_246143265.1 33778 - 35347 (+) NZ_PJAI02000001.1:346642-348211 -
- CWS31_RS17810 - 35518 - 35787 (+) NZ_PJAI02000001.1:348382-348651 -
- CWS31_RS01390 WP_148747650.1 35799 - 37086 (-) NZ_PJAI02000001.1:348663-349950 -
- CWS31_RS01395 WP_148747651.1 37397 - 38168 (-) NZ_PJAI02000001.1:350261-351032 -
- CWS31_RS01400 WP_148747652.1 38682 - 39795 (+) NZ_PJAI02000001.1:351546-352659 -
- CWS31_RS01405 WP_148747653.1 39807 - 40830 (+) NZ_PJAI02000001.1:352671-353694 -
- CWS31_RS01410 WP_148747678.1 40878 - 41643 (+) NZ_PJAI02000001.1:353742-354507 1.1.1.127
aldA CWS31_RS01415 WP_148747654.1 41649 - 43113 (+) NZ_PJAI02000001.1:354513-355977 1.2.1.-
- CWS31_RS01420 WP_148747655.1 43395 - 47793 (+) NZ_PJAI02000001.1:356259-360657 -
- CWS31_RS01430 WP_246143267.1 48337 - 49960 (+) NZ_PJAI02000001.1:361201-362824 -
- CWS31_RS01435 WP_211355772.1 50206 - 51625 (-) NZ_PJAI02000001.1:363070-364489 -
- CWS31_RS01440 WP_148747681.1 51699 - 53127 (-) NZ_PJAI02000001.1:364563-365991 -
- CWS31_RS01445 WP_148747656.1 53214 - 53910 (-) NZ_PJAI02000001.1:366078-366774 -
- CWS31_RS01450 WP_148747657.1 54148 - 54889 (-) NZ_PJAI02000001.1:367012-367753 -
- CWS31_RS01455 WP_148747658.1 54905 - 56459 (-) NZ_PJAI02000001.1:367769-369323 -
- CWS31_RS01460 WP_246143269.1 56586 - 59367 (-) NZ_PJAI02000001.1:369450-372231 -
- CWS31_RS01465 WP_148747659.1 59940 - 61062 (-) NZ_PJAI02000001.1:372804-373926 -
- CWS31_RS01470 WP_170252734.1 61587 - 62175 (-) NZ_PJAI02000001.1:374451-375039 -
- CWS31_RS01475 WP_148747661.1 62523 - 64890 (-) NZ_PJAI02000001.1:375387-377754 3.2.1.23
- CWS31_RS01480 WP_148747662.1 65362 - 69040 (+) NZ_PJAI02000001.1:378226-381904 -
- CWS31_RS01485 WP_148747663.1 69104 - 71249 (+) NZ_PJAI02000001.1:381968-384113 -
- CWS31_RS01490 WP_148747664.1 71710 - 73261 (+) NZ_PJAI02000001.1:384574-386125 -
- CWS31_RS01495 WP_148747665.1 73293 - 74013 (+) NZ_PJAI02000001.1:386157-386877 -
- CWS31_RS01500 WP_148747666.1 74227 - 76675 (-) NZ_PJAI02000001.1:387091-389539 -
- CWS31_RS01505 WP_148747667.1 76919 - 77339 (-) NZ_PJAI02000001.1:389783-390203 -
- CWS31_RS01510 WP_211355773.1 77341 - 78337 (-) NZ_PJAI02000001.1:390205-391201 -
- CWS31_RS01515 WP_211355774.1 78346 - 79369 (-) NZ_PJAI02000001.1:391210-392233 -
- CWS31_RS01520 WP_148747668.1 79397 - 80909 (-) NZ_PJAI02000001.1:392261-393773 7.5.2.-
- CWS31_RS01525 WP_148747669.1 80979 - 81939 (-) NZ_PJAI02000001.1:393843-394803 -
- CWS31_RS01530 WP_246143271.1 82129 - 85267 (-) NZ_PJAI02000001.1:394993-398131 -
- CWS31_RS01535 WP_148747670.1 85562 - 86504 (+) NZ_PJAI02000001.1:398426-399368 -
- CWS31_RS01540 WP_148747671.1 86684 - 87770 (+) NZ_PJAI02000001.1:399548-400634 -
- CWS31_RS01545 WP_101343344.1 87953 - 88994 (+) NZ_PJAI02000001.1:400817-401858 2.7.7.12
galK CWS31_RS01550 WP_101343345.1 89003 - 90170 (+) NZ_PJAI02000001.1:401867-403034 2.7.1.6
galE CWS31_RS01555 WP_101343346.1 90169 - 91195 (+) NZ_PJAI02000001.1:403033-404059 5.1.3.2
- CWS31_RS01560 WP_101343347.1 91194 - 92178 (+) NZ_PJAI02000001.1:404058-405042 5.1.3.-
- CWS31_RS01565 WP_101343348.1 92830 - 93991 (+) NZ_PJAI02000001.1:405694-406855 -
- CWS31_RS01570 WP_101343349.1 94068 - 94377 (+) NZ_PJAI02000001.1:406932-407241 -
- CWS31_RS01575 WP_101343350.1 94542 - 95802 (+) NZ_PJAI02000001.1:407406-408666 -

Cluster number

2

Gene name

Gene position

Gene type

Found by CGCFinder?

- 1 - 2574 (+) CAZyme: GH2| GH2 Yes (cluster 1)
- 2663 - 4225 (+) TC: gnl|TC-DB|P96169|2.A.21.3.2 Yes (cluster 1)
- 4454 - 6742 (+) other Yes (cluster 1)
fdhD 6923 - 7663 (+) other Yes (cluster 1)
- 7963 - 10251 (+) TC: gnl|TC-DB|P07658|3.D.1.9.2 Yes (cluster 1)
- 10327 - 11004 (+) other Yes (cluster 1)
- 11705 - 15667 (+) CAZyme: GH96|CBM6| GH96 Yes (cluster 1)
- 19929 - 21002 (-) other Yes (cluster 1)
- 21138 - 21899 (-) other Yes (cluster 1)
- 22166 - 23785 (-) TC: gnl|TC-DB|P96710|2.A.1.1.55 Yes (cluster 1)
- 24326 - 26698 (+) CAZyme: GH50|GH50 Yes (cluster 1)
- 26742 - 29012 (+) CAZyme: GH50|GH50 Yes (cluster 1)
- 29131 - 30843 (+) other Yes (cluster 1)
- 31299 - 33680 (+) CAZyme: GH50|GH50 Yes (cluster 1)
- 33779 - 35347 (+) CAZyme: GH29| GH29 Yes (cluster 1)
- 35800 - 37086 (-) STP: STP|SBP_bac_1 No
- 37398 - 38168 (-) TF: DBD-Pfam|TrmB No
- 38683 - 39795 (+) CDS No
- 39808 - 40830 (+) CDS No
- 40879 - 41643 (+) CDS No
aldA 41650 - 43113 (+) CDS No
- 43396 - 47793 (+) CDS No
- 48338 - 49960 (+) CDS No
- 50207 - 51625 (-) CDS No
- 51700 - 53127 (-) CDS No
- 53215 - 53910 (-) CDS No
- 54149 - 54889 (-) CDS No
- 54906 - 56459 (-) CDS No
- 56587 - 59367 (-) TC: gnl|TC-DB|Q9A608|1.B.14.12.1 Yes (cluster 2)
- 59941 - 61062 (-) other Yes (cluster 2)
- 61588 - 62175 (-) TF: DBD-Pfam|GntR,DBD-SUPERFAMILY|0039384 Yes (cluster 2)
- 62524 - 64890 (-) CAZyme: GH50|GH50 Yes (cluster 2)
- 65363 - 69040 (+) TC: gnl|TC-DB|Q9AAZ6|1.B.14.12.2 Yes (cluster 2)
- 69105 - 71249 (+) other Yes (cluster 2)
- 71711 - 73261 (+) other Yes (cluster 2)
- 73294 - 74013 (+) other Yes (cluster 2)
- 74228 - 76675 (-) CAZyme: GH86| GH86 Yes (cluster 2)
- 76920 - 77339 (-) other Yes (cluster 2)
- 77342 - 78337 (-) TC: gnl|TC-DB|A8H4W6|3.A.1.2.15 Yes (cluster 2)
- 78347 - 79369 (-) TC: gnl|TC-DB|Q0HIQ6|3.A.1.2.14 Yes (cluster 2)
- 79398 - 80909 (-) TC: gnl|TC-DB|Q8G847|3.A.1.2.23 Yes (cluster 2)
- 80980 - 81939 (-) TC: gnl|TC-DB|P39325|3.A.1.2.25 Yes (cluster 2)
- 82130 - 85267 (-) other Yes (cluster 2)
- 85563 - 86504 (+) STP: STP|PfkB Yes (cluster 2)
- 86685 - 87770 (+) CAZyme: GH117|GH117 Yes (cluster 2)
- 87954 - 88994 (+) CDS No
galK 89004 - 90170 (+) CDS No
galE 90170 - 91195 (+) CDS No
- 91195 - 92178 (+) CDS No
- 92831 - 93991 (+) CDS No
- 94069 - 94377 (+) CDS No
- 94543 - 95802 (+) STP: STP|Pyr_redox_2 No

PUL ID

PUL0652

PubMed

33811026, Appl Environ Microbiol. 2021 May 26;87(12):e0023021. doi: 10.1128/AEM.00230-21. Epub 2021 May 26.

Title

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

Author

Pathiraja D, Christiansen L, Park B, Schultz-Johansen M, Bang G, Stougaard P, Choi IG

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 alpha-agarases harbored in the agar-specific polysaccharide utilization locus (PUL) of Colwellia echini strain A3(T) facilitate the versatility of the agarolytic pathway. The cellular and molecular functions of the alpha-agarases examined by genomic, transcriptomic, and biochemical analyses revealed that alpha-agarases of C. echini A3(T) create a novel auxiliary pathway. alpha-Agarases convert even-numbered neoagarooligosaccharides to odd-numbered agaro- and 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 alpha-agarase, promote metabolic versatility by channeling agar metabolism through different routes. IMPORTANCEColwellia echini A3(T) 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 A3(T) encodes two alpha-agarases in addition to the core beta-agarolytic enzymes in its agarolytic PUL. Among the agar-degrading CAZymes identified so far, only a few alpha-agarases have been biochemically characterized. The molecular and biological functions of two alpha-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 alpha-agarolytic pathway in C. echini A3(T). The addition of alpha-agarases to the agarolytic enzyme repertoire might allow marine agarolytic bacteria to increase competitive abilities through metabolic versatility.