Characterization of a Hyaluronic Acid Utilization Locus and Identification of Two Hyaluronate Lyases in a Marine Bacterium Vibrio alginolyticus LWW-9.

Wengong Yu,Xiaoyi Wang,Hao Wu,Ziwei Wei,Feng Han,Yujiao Li

doi:10.3389/fmicb.2021.696096

Abstract

Hyaluronic acid (HA) is a negatively charged and linear polysaccharide existing in the tissues and body fluids of all vertebrates. Some pathogenic bacteria target hyaluronic acid for adhesion and/or infection to host cells. Vibrio alginolyticus is an opportunistic pathogen related to infections of humans and marine animals, and the hyaluronic acid-degrading potential of Vibrio spp. has been well-demonstrated. However, little is known about how Vibrio spp. utilize hyaluronic acid. In this study, a marine bacterium V. alginolyticus LWW-9 capable of degrading hyaluronic acid has been isolated. Genetic and bioinformatic analysis showed that V. alginolyticus LWW-9 harbors a gene cluster involved in the degradation, transport, and metabolism of hyaluronic acid. Two novel PL8 family hyaluronate lyases, VaHly8A and VaHly8B, are the key enzymes for the degradation of hyaluronic acid. VaHly8A and VaHly8B have distinct biochemical properties, reflecting the adaptation of the strain to the changing parameters of the aquatic habitats and hosts. Based on genomic and functional analysis, we propose a model for the complete degradation of hyaluronic acid by V. alginolyticus LWW-9. Overall, our study expands our knowledge of the HA utilization paradigm within the Proteobacteria, and the two novel hyaluronate lyases are excellent candidates for industrial applications.

Highlights

Animal cells are in close interaction with extracellular matrices (ECM), which function as a physical scaffold for organs and tissues, regulate various cellular functions and maintain homeostasis (Theocharis et al, 2016)
Hyaluronate lyases are categorized into four polysaccharide lyase (PL) families, PL8, PL16, PL30, and PL33, in the Carbohydrate-Active Enzymes (CAZy) database according to primary structures (Lombard et al, 2014)
Sixteen type strains in Vibrio were selected for phylogenetic analysis, and the result showed that strain LWW-9 was closest to V. alginolyticus strain ATCC 17749 (NR_118258.1) in the phylogenetic tree (Figure 1)

Summary

INTRODUCTION

Animal cells are in close interaction with extracellular matrices (ECM), which function as a physical scaffold for organs and tissues, regulate various cellular functions and maintain homeostasis (Theocharis et al, 2016). Due to its excellent physicochemical characteristics, HA has a variety of applications in the pharmaceutical industry, such as orthopedics, ophthalmology, and aesthetic dermatology (Sudha and Rose, 2014) Some pathogenic bacteria, such as streptococci and streptobacillus, produce extracellular or cell-surface hyaluronate lyase to depolymerize HA, facilitating the invasion of the host (Li and Jedrzejas, 2001; Oiki et al, 2017). We isolated a hyaluronate lyase-producing bacterium, Vibrio alginolyticus strain LWW-9. We provided a model for how V. alginolyticus strain LWW-9 utilizes the HA. These results presented here not merely extend our understanding of the HA utilization paradigm within the Proteobacteria and may contribute to the elucidation of bacterial physiology and pathogenicity

MATERIALS AND METHODS

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT