Functional metagenomics reveals differential chitin degradation and utilization features across free-living and host-associated marine microbiomes

I Raimundo,R Silva,R Costa,A Lago-Lestón,L Meunier,T Keller-Costa,S M Valente

doi:10.1186/s40168-020-00970-2

Abstract

BackgroundChitin ranks as the most abundant polysaccharide in the oceans yet knowledge of shifts in structure and diversity of chitin-degrading communities across marine niches is scarce. Here, we integrate cultivation-dependent and -independent approaches to shed light on the chitin processing potential within the microbiomes of marine sponges, octocorals, sediments, and seawater.ResultsWe found that cultivatable host-associated bacteria in the genera Aquimarina, Enterovibrio, Microbulbifer, Pseudoalteromonas, Shewanella, and Vibrio were able to degrade colloidal chitin in vitro. Congruent with enzymatic activity bioassays, genome-wide inspection of cultivated symbionts revealed that Vibrio and Aquimarina species, particularly, possess several endo- and exo-chitinase-encoding genes underlying their ability to cleave the large chitin polymer into oligomers and dimers. Conversely, Alphaproteobacteria species were found to specialize in the utilization of the chitin monomer N-acetylglucosamine more often. Phylogenetic assessments uncovered a high degree of within-genome diversification of multiple, full-length endo-chitinase genes for Aquimarina and Vibrio strains, suggestive of a versatile chitin catabolism aptitude. We then analyzed the abundance distributions of chitin metabolism-related genes across 30 Illumina-sequenced microbial metagenomes and found that the endosymbiotic consortium of Spongia officinalis is enriched in polysaccharide deacetylases, suggesting the ability of the marine sponge microbiome to convert chitin into its deacetylated—and biotechnologically versatile—form chitosan. Instead, the abundance of endo-chitinase and chitin-binding protein-encoding genes in healthy octocorals leveled up with those from the surrounding environment but was found to be depleted in necrotic octocoral tissue. Using cultivation-independent, taxonomic assignments of endo-chitinase encoding genes, we unveiled previously unsuspected richness and divergent structures of chitinolytic communities across host-associated and free-living biotopes, revealing putative roles for uncultivated Gammaproteobacteria and Chloroflexi symbionts in chitin processing within sessile marine invertebrates.ConclusionsOur findings suggest that differential chitin degradation pathways, utilization, and turnover dictate the processing of chitin across marine micro-niches and support the hypothesis that inter-species cross-feeding could facilitate the co-existence of chitin utilizers within marine invertebrate microbiomes. We further identified chitin metabolism functions which may serve as indicators of microbiome integrity/dysbiosis in corals and reveal putative novel chitinolytic enzymes in the genus Aquimarina that may find applications in the blue biotechnology sector.4kjGuZRPCftKy_HwBHqQX8Video abstract

Highlights

Chitin ranks as the most abundant polysaccharide in the oceans yet knowledge of shifts in structure and diversity of chitin-degrading communities across marine niches is scarce
Our findings suggest that differential chitin degradation pathways, utilization, and turnover dictate the processing of chitin across marine micro-niches and support the hypothesis that inter-species cross-feeding could facilitate the co-existence of chitin utilizers within marine invertebrate microbiomes
We further identified chitin metabolism functions which may serve as indicators of microbiome integrity/dysbiosis in corals and reveal putative novel chitinolytic enzymes in the genus Aquimarina that may find applications in the blue biotechnology sector

Summary

Introduction

Chitin ranks as the most abundant polysaccharide in the oceans yet knowledge of shifts in structure and diversity of chitin-degrading communities across marine niches is scarce. Chitin does not accumulate in marine habitats as it is hydrolyzed by microorganisms that can use it as a carbon, nitrogen, and/or energy source [2] This process is often mediated by chitinolytic enzymes, named chitinases, that hydrolyze the β-1,4 glycosidic bonds between the GlcNAc residues, producing chito-oligosaccharides (COSs). The chitin derivative chitosan, formed via deacetylation, can be as well partially hydrolyzed by endo-chitinases if acetylated units remain in the polymer. Both endo- and exo-chitinases and their products have properties that bear promise for the development of new appliances in the food, medical, and agricultural sectors Both endo- and exo-chitinases and their products have properties that bear promise for the development of new appliances in the food, medical, and agricultural sectors (for an overview see refs. [5,6,7,8,9,10,11,12])

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