The Fish Pathogen Aliivibrio salmonicida LFI1238 Can Degrade and Metabolize Chitin despite Gene Disruption in the Chitinolytic Pathway

Autor: Sophanit Mekasha, Anna Skåne, Geir Mathiesen, Gustav Vaaje-Kolstad, Jennifer S. M. Loose, Magnus Ø. Arntzen, Bastien Bissaro, Giusi Minniti
Přispěvatelé: Norwegian University of Life Sciences (NMBU), European Project: 249865,EC:FP7:PEOPLE,FP7-PEOPLE-2009-RG,PLANTPEPTIDOMICS(2010), European Project: 267196,EC:FP7:PEOPLE,FP7-PEOPLE-2010-COFUND,AGREENSKILLS(2012)
Jazyk: angličtina
Rok vydání: 2021
Předmět:
[SDV]Life Sciences [q-bio]
Chitin
Polysaccharide
Disaccharides
Applied Microbiology and Biotechnology
Aliivibrio salmonicida
Microbiology
Acetylglucosamine
Mixed Function Oxygenases
chitinaselytic polysaccharide monooxygenase
03 medical and health sciences
chemistry.chemical_compound
0302 clinical medicine
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]

Aliivibrio
Animals
Enzymology and Protein Engineering
Pathogen
Glycoside hydrolase family 18
030304 developmental biology
chemistry.chemical_classification
0303 health sciences
Ecology
biology
Chitinases
Fishes
biology.organism_classification
PMO
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
Vibrio
carbohydrates (lipids)
chemistry
Chitinase
biology.protein
[SDV.AEN]Life Sciences [q-bio]/Food and Nutrition
030217 neurology & neurosurgery
Bacteria
Food Science
Biotechnology
Signal Transduction
pathogen
Zdroj: Applied and Environmental Microbiology
Applied and Environmental Microbiology, American Society for Microbiology, 2021, 87 (19), 25 p. ⟨10.1128/AEM.00529-21⟩
Appl Environ Microbiol
ISSN: 0099-2240
1098-5336
DOI: 10.1128/AEM.00529-21⟩
Popis: The fish pathogen Aliivibrio (Vibrio) salmonicida LFI1238 is thought to be incapable of utilizing chitin as a nutrient source, since approximately half of the genes representing the chitinolytic pathway are disrupted by insertion sequences. In the present study, we combined a broad set of analytical methods to investigate this hypothesis. Cultivation studies revealed that A. salmonicida grew efficiently on N-acetylglucosamine (GlcNAc) and chitobiose [(GlcNAc)(2)], the primary soluble products resulting from enzymatic chitin hydrolysis. The bacterium was also able to grow on chitin particles, albeit at a lower rate than on the soluble substrates. The genome of the bacterium contains five disrupted chitinase genes (pseudogenes) and three intact genes encoding a glycoside hydrolase family 18 (GH18) chitinase and two auxiliary activity family 10 (AA10) lytic polysaccharide monooxygenases (LPMOs). Biochemical characterization showed that the chitinase and LPMOs were able to depolymerize both α- and β-chitin to (GlcNAc)(2) and oxidized chitooligosaccharides, respectively. Notably, the chitinase displayed up to 50-fold lower activity than other well-studied chitinases. Deletion of the genes encoding the intact chitinolytic enzymes showed that the chitinase was important for growth on β-chitin, whereas the LPMO gene deletion variants only showed minor growth defects on this substrate. Finally, proteomic analysis of A. salmonicida LFI1238 growth on β-chitin showed expression of all three chitinolytic enzymes and, intriguingly, also three of the disrupted chitinases. In conclusion, our results show that A. salmonicida LFI1238 can utilize chitin as a nutrient source and that the GH18 chitinase and the two LPMOs are needed for this ability. IMPORTANCE The ability to utilize chitin as a source of nutrients is important for the survival and spread of marine microbial pathogens in the environment. One such pathogen is Aliivibrio (Vibrio) salmonicida, the causative agent of cold water vibriosis. Due to extensive gene decay, many key enzymes in the chitinolytic pathway have been disrupted, putatively rendering this bacterium incapable of chitin degradation and utilization. In the present study, we demonstrate that A. salmonicida can degrade and metabolize chitin, the most abundant biopolymer in the ocean. Our findings shed new light on the environmental adaption of this fish pathogen.
Databáze: OpenAIRE