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Cite: NAR/gkaa742 2020



PUL General Information

Literature Information

PUL ID

PUL0458

PubMed

31915221, mSphere. 2020 Jan 8;5(1):e00792-19. doi: 10.1128/mSphere.00792-19.

Characterization method

RNA-Seq,analysis of reaction products,enzyme activity assay

Genomic accession number

NZ_PJAI02000005.1

Nucelotide position range

97665-174649

Substrate

carrageenan

Loci

CWS31_RS06455-CWS31_RS06695

Species

Colwellia echini/1982103

Degradation or Biosynthesis

degradation

Gene Name

Locus Tag

Protein ID

Gene Position

GenBank Contig Range

EC Number

- CWS31_RS06455 WP_148747692.1 97665 - 98655 (-) NZ_PJAI02000005.1:195330-196320 -
- CWS31_RS06460 WP_148747693.1 98832 - 100599 (-) NZ_PJAI02000005.1:196497-198264 -
- CWS31_RS06465 WP_148747694.1 100730 - 104360 (-) NZ_PJAI02000005.1:198395-202025 -
- CWS31_RS06470 WP_148747695.1 104897 - 106337 (-) NZ_PJAI02000005.1:202562-204002 -
- CWS31_RS06475 WP_148747696.1 106333 - 107485 (-) NZ_PJAI02000005.1:203998-205150 -
- CWS31_RS06480 WP_148747735.1 108208 - 108598 (-) NZ_PJAI02000005.1:205873-206263 -
- CWS31_RS06485 WP_148747697.1 108754 - 109372 (-) NZ_PJAI02000005.1:206419-207037 -
- CWS31_RS06490 WP_148747698.1 109365 - 110232 (-) NZ_PJAI02000005.1:207030-207897 -
- CWS31_RS06495 WP_148747699.1 110348 - 111245 (+) NZ_PJAI02000005.1:208013-208910 -
- CWS31_RS06500 WP_148747700.1 111970 - 112399 (-) NZ_PJAI02000005.1:209635-210064 -
- CWS31_RS06505 WP_148747701.1 112517 - 113297 (-) NZ_PJAI02000005.1:210182-210962 1.1.1.47
- CWS31_RS06510 WP_148747736.1 113517 - 115083 (+) NZ_PJAI02000005.1:211182-212748 -
- CWS31_RS06515 WP_148747702.1 115177 - 116086 (+) NZ_PJAI02000005.1:212842-213751 -
- CWS31_RS06520 WP_148747703.1 116090 - 116726 (+) NZ_PJAI02000005.1:213755-214391 4.1.2.21
- CWS31_RS06525 WP_148747704.1 116820 - 117990 (+) NZ_PJAI02000005.1:214485-215655 -
- CWS31_RS06530 WP_148747705.1 118253 - 119000 (-) NZ_PJAI02000005.1:215918-216665 -
- CWS31_RS06535 WP_148747706.1 119627 - 121475 (+) NZ_PJAI02000005.1:217292-219140 -
- CWS31_RS06540 WP_148747707.1 121760 - 123230 (+) NZ_PJAI02000005.1:219425-220895 -
- CWS31_RS06545 WP_148747708.1 123517 - 125293 (-) NZ_PJAI02000005.1:221182-222958 -
- CWS31_RS06550 WP_148747709.1 125636 - 126068 (+) NZ_PJAI02000005.1:223301-223733 -
- CWS31_RS06560 WP_148747711.1 126752 - 129083 (+) NZ_PJAI02000005.1:224417-226748 -
- CWS31_RS06570 WP_148747712.1 129524 - 131552 (-) NZ_PJAI02000005.1:227189-229217 -
- CWS31_RS06575 WP_148747713.1 131811 - 132336 (+) NZ_PJAI02000005.1:229476-230001 -
- CWS31_RS06580 WP_148747737.1 132596 - 133361 (-) NZ_PJAI02000005.1:230261-231026 -
- CWS31_RS06585 WP_148747714.1 133535 - 134450 (-) NZ_PJAI02000005.1:231200-232115 -
- CWS31_RS06590 WP_148747715.1 134530 - 135439 (-) NZ_PJAI02000005.1:232195-233104 -
- CWS31_RS06595 WP_148747716.1 135853 - 137530 (+) NZ_PJAI02000005.1:233518-235195 -
- CWS31_RS06600 WP_148747717.1 137529 - 138420 (+) NZ_PJAI02000005.1:235194-236085 -
- CWS31_RS06605 WP_148747738.1 138439 - 139219 (+) NZ_PJAI02000005.1:236104-236884 -
- CWS31_RS06610 WP_148747718.1 139331 - 140936 (+) NZ_PJAI02000005.1:236996-238601 -
- CWS31_RS06615 WP_148747719.1 140958 - 142137 (+) NZ_PJAI02000005.1:238623-239802 -
- CWS31_RS06620 WP_148747720.1 142746 - 143721 (-) NZ_PJAI02000005.1:240411-241386 -
- CWS31_RS06625 WP_148747721.1 144055 - 145513 (+) NZ_PJAI02000005.1:241720-243178 -
- CWS31_RS06630 WP_148747722.1 146011 - 146986 (-) NZ_PJAI02000005.1:243676-244651 -
- CWS31_RS06635 WP_148747723.1 147106 - 149455 (-) NZ_PJAI02000005.1:244771-247120 -
- CWS31_RS06645 WP_148747725.1 150443 - 154157 (-) NZ_PJAI02000005.1:248108-251822 -
- CWS31_RS06650 WP_148747726.1 154747 - 155851 (-) NZ_PJAI02000005.1:252412-253516 -
- CWS31_RS06655 WP_148747727.1 156553 - 158461 (-) NZ_PJAI02000005.1:254218-256126 -
- CWS31_RS06660 WP_148747728.1 158523 - 160506 (-) NZ_PJAI02000005.1:256188-258171 -
- CWS31_RS06665 WP_148747729.1 160557 - 161700 (-) NZ_PJAI02000005.1:258222-259365 -
- CWS31_RS06670 WP_148747730.1 161823 - 163308 (-) NZ_PJAI02000005.1:259488-260973 -
- CWS31_RS06675 WP_148747739.1 163419 - 164937 (-) NZ_PJAI02000005.1:261084-262602 -
- CWS31_RS06680 WP_148747731.1 165823 - 168274 (-) NZ_PJAI02000005.1:263488-265939 -
- CWS31_RS06685 WP_148747732.1 168472 - 170749 (-) NZ_PJAI02000005.1:266137-268414 -
- CWS31_RS06690 WP_148747733.1 170874 - 173523 (-) NZ_PJAI02000005.1:268539-271188 -
- CWS31_RS06695 WP_101344349.1 173896 - 174649 (+) NZ_PJAI02000005.1:271561-272314 -

Cluster number

1

Gene name

Gene position

Gene type

Found by CGCFinder?

- 97666 - 98655 (-) CAZyme: GH16 Yes
- 98833 - 100599 (-) other Yes
- 100731 - 104360 (-) other Yes
- 104898 - 106337 (-) other Yes
- 106334 - 107485 (-) other Yes
- 108209 - 108598 (-) other Yes
- 108755 - 109372 (-) other Yes
- 109366 - 110232 (-) other Yes
- 110349 - 111245 (+) TF: DBD-Pfam|HTH_1 Yes
- 111971 - 112399 (-) other Yes
- 112518 - 113297 (-) other Yes
- 113518 - 115083 (+) TC: gnl|TC-DB|Q8NTX0|2.A.1.1.53 Yes
- 115178 - 116086 (+) other Yes
- 116091 - 116726 (+) other Yes
- 116821 - 117990 (+) other Yes
- 118254 - 119000 (-) TF: DBD-Pfam|GntR,DBD-SUPERFAMILY|0037767 Yes
- 119628 - 121475 (+) other Yes
- 121761 - 123230 (+) other Yes
- 123518 - 125293 (-) other Yes
- 125637 - 126068 (+) other Yes
- 126210 - 126602 (+) other Yes
- 126753 - 129083 (+) CAZyme: GH16|CBM16 Yes
- 129190 - 129385 (-) other Yes
- 129525 - 131552 (-) TC: gnl|TC-DB|M3JA40|1.B.52.2.1 Yes
- 131812 - 132336 (+) other Yes
- 132597 - 133361 (-) TF: DBD-Pfam|TrmB,DBD-SUPERFAMILY|0040266 Yes
- 133536 - 134450 (-) other Yes
- 134531 - 135439 (-) CAZyme: GH16 Yes
- 135854 - 137530 (+) TC: gnl|TC-DB|Q5E733|2.A.21.3.7 Yes
- 137530 - 138420 (+) CDS No
- 138440 - 139219 (+) CDS No
- 139332 - 140936 (+) CDS No
- 140959 - 142137 (+) CDS No
- 142747 - 143721 (-) CDS No
- 144056 - 145513 (+) CDS No
- 146012 - 146986 (-) CDS No
- 147107 - 149455 (-) CDS No
- 150016 - 150192 (-) CDS No
- 150444 - 154157 (-) CDS No
- 154748 - 155851 (-) CDS No
- 156554 - 158461 (-) CDS No
- 158524 - 160506 (-) CDS No
- 160558 - 161700 (-) CAZyme: GH16 No
- 161824 - 163308 (-) CDS No
- 163420 - 164937 (-) CDS No
- 165824 - 168274 (-) CDS No
- 168473 - 170749 (-) CDS No
- 170875 - 173523 (-) CDS No
- 173897 - 174649 (+) TF: DBD-Pfam|GntR,DBD-SUPERFAMILY|0043758 No

PUL ID

PUL0458

PubMed

31915221, mSphere. 2020 Jan 8;5(1):e00792-19. doi: 10.1128/mSphere.00792-19.

Title

A Multifunctional Polysaccharide Utilization Gene Cluster in Colwellia echini Encodes Enzymes for the Complete Degradation of kappa-Carrageenan, iota-Carrageenan, and Hybrid beta/kappa-Carrageenan.

Author

Christiansen L, Pathiraja D, Bech PK, Schultz-Johansen M, Hennessy R, Teze D, Choi IG, Stougaard P

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 A3(T) is a potent enzyme producer since it completely hydrolyzes agar and kappa-carrageenan. Here, we report that the genome of C. echini A3(T) 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 beta- and kappa-carrageenan motifs. We show that furcellaranases degrade furcellaran into neocarratetraose-43-O-monosulfate [DA-(alpha1,3)-G4S-(beta1,4)-DA-(alpha1,3)-G], and we propose a molecular model of furcellaranases and compare the active site architectures of furcellaranases, kappa-carrageenases, beta-agarases, and beta-porphyranases. Furthermore, C. echini A3(T) was shown to encode kappa-carrageenases, iota-carrageenases, and members of a new class of enzymes, active only on hybrid beta/kappa-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 A3(T) degrades complex sulfated marine polysaccharides such as furcellaran, kappa-carrageenan, and iota-carrageenan.IMPORTANCE Here, we report that a recently described bacterium, Colwellia echini, harbors a large number of enzymes enabling the bacterium to grow on kappa-carrageenan and agar. The genes are organized in two clusters that encode enzymes for the total degradation of kappa-carrageenan and agar, respectively. As the first, we report on the structure/function relationship of a new class of enzymes that hydrolyze furcellaran, a partially sulfated beta/kappa-carrageenan. Using an in silico model, we hypothesize a molecular structure of furcellaranases and compare structural features and active site architectures of furcellaranases with those of other GH16 polysaccharide hydrolases, such as kappa-carrageenases, beta-agarases, and beta-porphyranases. Furthermore, we describe a new class of enzymes distantly related to GH42 and GH160 beta-galactosidases and show that this new class of enzymes is active only on hybrid beta/kappa-carrageenan oligosaccharides. Finally, we propose a new model for how the carrageenolytic enzyme repertoire enables C. echini to metabolize beta/kappa-, kappa-, and iota-carrageenan.