Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria

Ficko-Blean, E.; Préchoux, Aurélie; Thomas, François; Rochat, Tatiana; Larocque, Robert; Zhu, Yongtao; Stam, Mark; Genicot, Sabine; Jam, Murielle; Calteau, Alexandra; Viart, Benjamin Thomas; Ropartz, David; Pérez-Pascual, David; Correc, Gaëlle; Matard-Mann, Maria; Stubbs, Keith A.; Rogniaux, Hélène; Jeudy, Alexandra; Barbeyron, Tristan; Médigue, Claudine; Czjzek, Mirjam; Vallenet, David; McBride, Mark J.; Duchaud, Éric; Michel, Gurvan

doi:10.1038/s41467-017-01832-6

Cited by 137 publications

(181 citation statements)

References 78 publications

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“…In members of Bacteroidetes, these assemblages are known as Polysaccharide Utilization Loci (PULs) [40], and are recognized by the existence of tandem SusC/SusD transporter systems. Similar gene constellations absent of canonical SusC/SusD pairs have been reported in other phyla as well, including Gammaproteobacteria [41,42], and have recently lead to an update of the PUL term [40,42]. Closer inspection of contig 58 showed that the identified GH107 fucanase genes (fp273, fp277, and fp279) displayed such an organization ( Fig.…”

Section: Sequence Analysis Of Three Novel Endo-fucanases Provides Newsupporting

confidence: 72%

“…Despite increased activities in next‐generation sequencing of the marine environment , public databases contain relatively few GH107 candidates. This small number is in contrast to CAZymes targeting other algal polysaccharides (e.g., carrageenases and alginate lyases), which are often highly abundant in the public databases . One possibility could be that bacteria carrying GH107s are specific to certain ecological niches, which have not been frequently investigated.…”

Section: Resultsmentioning

confidence: 99%

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Discovery and screening of novel metagenome‐derived GH107 enzymes targeting sulfated fucans from brown algae

et al. 2018

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Sulfated fucans, often denoted as fucoidans, are highly variable cell wall polysaccharides of brown algae, which possess a wide range of bioactive properties with potential pharmaceutical applications. Due to their complex architecture, the structures of algal fucans have until now only been partly determined. Enzymes capable of hydrolyzing sulfated fucans may allow specific release of defined bioactive oligosaccharides and may serve as a tool for structural elucidation of algal walls. Currently, such enzymes include only a few hydrolases belonging to the glycoside hydrolase family 107 (GH107), and little is known about their mechanistics and the substrates they degrade. In this study, we report the identification and recombinant production of three novel GH107 family proteins derived from a marine metagenome. Activity screening against a large substrate collection showed that all three enzymes degraded sulfated fucans from brown algae in the order Fucales. This is in accordance with a hydrolytic activity against α-1,4-fucosidic linkages in sulfated fucans as reported for previous GH107 members. Also, the activity screening gave new indications about the structural differences in brown algal cell walls. Finally, sequence analyses allowed identification of the proposed catalytic residues of the GH107 family. The findings presented here form a new basis for understanding the GH107 family of enzymes and investigating the complex sulfated fucans from brown algae. DATABASE: The assembled metagenome and raw sequence data is available at EMBL-EBI (Study number: PRJEB28480). Sequences of the GH107 fucanases (Fp273, Fp277, and Fp279) have been deposited in GenBank under accessions MH755451-MH755453.

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Section: Sequence Analysis Of Three Novel Endo-fucanases Provides Newsupporting

confidence: 72%

Section: Resultsmentioning

confidence: 99%

Discovery and screening of novel metagenome‐derived GH107 enzymes targeting sulfated fucans from brown algae

et al. 2018

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“…A pathway for the degradation of -carrageenan in strain A3 T showed similarity to the pathways in P. carrageenovora 9 T (29) and Z. galactanivorans (20). The -carrageenase Ce391 and possibly Ce392 hydrolyze -carrageenan to -neocarrabiose (DA2S-G4S), which subsequently may be desulfated by a DA2S sulfatase and a G4S sulfatase.…”

Section: Resultsmentioning

confidence: 81%

“…1). TonB-dependent receptors, previously proposed to be analogous to the Bacteroidetes detection system (10,19,20), were located in both gene clusters (Ce2863 and Ce345; Fig. 1).…”

Section: Resultsmentioning

confidence: 88%

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

Christiansen

Pathiraja

Bech

et al. 2020

mSphere

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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 -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 ␤and -carrageenan motifs. We show that furcellaranases degrade furcellaran into neocarratetraose-43-O-monosulfate [DA-(␣1,3)-G4S-(␤1,4)-DA-(␣1,3)-G], and we propose a molecular model of furcellaranases and compare the active site architectures of furcellaranases, -carrageenases, ␤-agarases, and ␤-porphyranases. Furthermore, C. echini A3 T was shown to encode -carrageenases, -carrageenases, and members of a new class of enzymes, active only on hybrid ␤/-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, -carrageenan, and -carrageenan. IMPORTANCE Here, we report that a recently described bacterium, Colwellia echini, harbors a large number of enzymes enabling the bacterium to grow on -carrageenan and agar. The genes are organized in two clusters that encode enzymes for the total degradation of -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 ␤/-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 -carrageenases, ␤-agarases, and ␤-porphyranases. Furthermore, we describe a new class of enzymes distantly related to GH42 and GH160 ␤-galactosidases and show that this new class of enzymes is active only on hybrid ␤/-carrageenan oligosaccharides. Finally, we propose a new model for how the carrageenolytic enzyme repertoire enables C. echini to metabolize ␤/-, -, and -carrageenan.

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“…Accessory genes, such as transcriptional regulators, transporter genes and sulfatases, are also often encoded by PULs. Recent studies showed the remarkable repertoires of CAZymes of Flavobacteriia (Hehemann et al ., ; Thomas et al ., ; Ficko‐Blean et al ., ), which are frequently associated with algae blooms (Teeling et al ., ; Williams et al ., ; Teeling et al ., ). Due to the large chemical diversity of algal polysaccharides, individual bacterial strains have adapted to utilize only selected polysaccharide subsets as energy and carbon sources (Landa et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Alpha‐ and beta‐mannan utilization by marine Bacteroidetes

Chen

Robb

Unfried

et al. 2018

Environmental Microbiology

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Summary Marine microscopic algae carry out about half of the global carbon dioxide fixation into organic matter. They provide organic substrates for marine microbes such as members of the Bacteroidetes that degrade algal polysaccharides using carbohydrate‐active enzymes (CAZymes). In Bacteroidetes genomes CAZyme encoding genes are mostly grouped in distinct regions termed polysaccharide utilization loci (PULs). While some studies have shown involvement of PULs in the degradation of algal polysaccharides, the specific substrates are for the most part still unknown. We investigated four marine Bacteroidetes isolated from the southern North Sea that harbour putative mannan‐specific PULs. These PULs are similarly organized as PULs in human gut Bacteroides that digest α‐ and β‐mannans from yeasts and plants respectively. Using proteomics and defined growth experiments with polysaccharides as sole carbon sources we could show that the investigated marine Bacteroidetes express the predicted functional proteins required for α‐ and β‐mannan degradation. Our data suggest that algal mannans play an as yet unknown important role in the marine carbon cycle, and that biochemical principles established for gut or terrestrial microbes also apply to marine bacteria, even though their PULs are evolutionarily distant.

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Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria

Cited by 137 publications

References 78 publications

Discovery and screening of novel metagenome‐derived GH107 enzymes targeting sulfated fucans from brown algae

Discovery and screening of novel metagenome‐derived GH107 enzymes targeting sulfated fucans from brown algae

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

Alpha‐ and beta‐mannan utilization by marine Bacteroidetes

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