The catabolic specialization of the marine bacterium Polaribacter sp. Q13 to red algal β1,3/1,4-mixed-linkage xylan

Author:

Zhao Fang1ORCID,Yu Chun-Mei1,Sun Hai-Ning1,Xu Ting-Ting1,Sun Zhong-Zhi1,Qin Qi-Long1,Wang Ning1ORCID,Chen Xiu-Lan123ORCID,Yu Yang1ORCID,Zhang Yu-Zhong123ORCID

Affiliation:

1. Marine Biotechnology Research Center, State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China

2. College of Marine Life Sciences & Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China

3. Laboratory for Marine Biology and Biotechnology, Laoshan Laboratory, Qingdao, China

Abstract

ABSTRACT Catabolism of algal polysaccharides by marine bacteria is a significant process of marine carbon cycling. β1,3/1,4 - Mixed-linkage xylan (MLX) is a class of xylan in the ocean, widely present in the cell walls of red algae. However, the catabolic mechanism of MLX by marine bacteria remains elusive. Recently, we found that a marine Bacteroidetes strain, Polaribacter sp. Q13, is a specialist in degrading MLX, which secretes a novel MLX-specific xylanase. Here, the catabolic specialization of strain Q13 to MLX was studied by multiomics and biochemical analyses. Strain Q13 catabolizes MLX with a canonical starch utilization system (Sus), which is encoded by a single xylan utilization locus, XUL-Q13. In this system, the cell surface glycan-binding protein SGBP-B captures MLX specifically, contributing to the catabolic specificity. The xylanolytic enzyme system of strain Q13 is unique, and the enzymatic cascade dedicates the stepwise hydrolysis of the β1,3- and β1,4-linkages in MLX in the extracellular, periplasmic, and cytoplasmic spaces. Bioinformatics analysis and growth observation suggest that other marine Bacteroidetes strains harboring homologous MLX utilization loci also preferentially utilize MLX. These results reveal the catabolic specialization of MLX degradation by marine Bacteroidetes, leading to a better understanding of the degradation and recycling of MLX driven by marine bacteria. IMPORTANCE Red algae contribute substantially to the primary production in marine ecosystems. The catabolism of red algal polysaccharides by marine bacteria is important for marine carbon cycling. Mixed-linkage β1,3/1,4-xylan (MLX, distinct from hetero-β1,4-xylans from terrestrial plants) is an abundant red algal polysaccharide, whose mechanism of catabolism by marine bacteria, however, remains largely unknown. This study reveals the catabolism of MLX by marine Bacteroidetes, promoting our understanding of the degradation and utilization of algal polysaccharides by marine bacteria. This study also sets a foundation for the biomass conversion of MLX.

Funder

MOST | National Key Research and Development Program of China

Marine S&T Fund of Shandong Province for Qingdao Marine Science and Technology Center

National Science Foundation

Program of Shandong foTaishan Scholars

山东省科学技术厅 | Natural Science Foundation of Shandong Province

Publisher

American Society for Microbiology

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