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

02/14/2021

<jats:title>Abstract</jats:title><jats:sec><jats:title>Background</jats:title><jats:p>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. 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.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>We found that cultivatable host-associated bacteria in the genera<jats:italic>Aquimarina</jats:italic>,<jats:italic>Enterovibrio</jats:italic>,<jats:italic>Microbulbifer</jats:italic>,<jats:italic>Pseudoalteromonas</jats:italic>,<jats:italic>Shewanella</jats:italic>, and<jats:italic>Vibrio</jats:italic>were able to degrade colloidal chitin in vitro. Congruent with enzymatic activity bioassays, genome-wide inspection of cultivated symbionts revealed that<jats:italic>Vibrio</jats:italic>and<jats:italic>Aquimarina</jats:italic>species, particularly, possess several endo- and exo-chitinase-encoding genes underlying their ability to cleave the large chitin polymer into oligomers and dimers. Conversely,<jats:italic>Alphaproteobacteria</jats:italic>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<jats:italic>Aquimarina</jats:italic>and<jats:italic>Vibrio</jats:italic>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<jats:italic>Spongia officinalis</jats:italic>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<jats:italic>Gammaproteobacteria</jats:italic>and<jats:italic>Chloroflexi</jats:italic>symbionts in chitin processing within sessile marine invertebrates.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>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<jats:italic>Aquimarina</jats:italic>that may find applications in the blue biotechnology sector.</jats:p></jats:sec>

Authors in the community:

• 

  T

  Tina Keller Costa

  ist427891

  Affiliations and sources

  IST > iBB

  Instituto de Bioengenharia e Biociências

  In: orcid

  ID: 89422082

VoR - Version of Record

Springer Science and Business Media LLC

Microbiome

9

1

2049-2618

10.1186/s40168-020-00970-2

biological-sciences - Biological sciences

Keywords

• Microbiology (medical)
• Microbiology

eng - English