Polymeric carbohydrates utilization separates microbiomes into niches: insights into the diversity of microbial carbohydrate-active enzymes in the inner shelf of the Pearl River Estuary, China

Cui-Ci Sun; Wen-Jie Zhao; Wei-Zhong Yue; Hao Cheng; Fu-Lin Sun; Yu-Tu Wang; Mei-Lin Wu; Anja Engel; You-Shao Wang

doi:10.3389/fmicb.2023.1180321

Polymeric carbohydrates utilization separates microbiomes into niches: insights into the diversity of microbial carbohydrate-active enzymes in the inner shelf of the Pearl River Estuary, China

Front Microbiol. 2023 Jun 21:14:1180321. doi: 10.3389/fmicb.2023.1180321. eCollection 2023.

Authors

Cui-Ci Sun^{1

2}, Wen-Jie Zhao^{1

3}, Wei-Zhong Yue¹, Hao Cheng¹, Fu-Lin Sun^{1

2}, Yu-Tu Wang², Mei-Lin Wu¹, Anja Engel⁴, You-Shao Wang^{1

2}

Affiliations

¹ State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
² Daya Bay Marine Biology Research Station, Chinese Academy of Sciences, Shenzhen, China.
³ University of Chinese Academy of Sciences, Beijing, China.
⁴ GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.

Abstract

Polymeric carbohydrates are abundant and their recycling by microbes is a key process of the ocean carbon cycle. A deeper analysis of carbohydrate-active enzymes (CAZymes) can offer a window into the mechanisms of microbial communities to degrade carbohydrates in the ocean. In this study, metagenomic genes encoding microbial CAZymes and sugar transporter systems were predicted to assess the microbial glycan niches and functional potentials of glycan utilization in the inner shelf of the Pearl River Estuary (PRE). The CAZymes gene compositions were significantly different between in free-living (0.2-3 μm, FL) and particle-associated (>3 μm, PA) bacteria of the water column and between water and surface sediments, reflecting glycan niche separation on size fraction and selective degradation in depth. Proteobacteria and Bacteroidota had the highest abundance and glycan niche width of CAZymes genes, respectively. At the genus level, Alteromonas (Gammaproteobacteria) exhibited the greatest abundance and glycan niche width of CAZymes genes and were marked by a high abundance of periplasmic transporter protein TonB and members of the major facilitator superfamily (MFS). The increasing contribution of genes encoding CAZymes and transporters for Alteromonas in bottom water contrasted to surface water and their metabolism are tightly related with particulate carbohydrates (pectin, alginate, starch, lignin-cellulose, chitin, and peptidoglycan) rather than on the utilization of ambient-water DOC. Candidatus Pelagibacter (Alphaproteobacteria) had a narrow glycan niche and was primarily preferred for nitrogen-containing carbohydrates, while their abundant sugar ABC (ATP binding cassette) transporter supported the scavenging mode for carbohydrate assimilation. Planctomycetota, Verrucomicrobiota, and Bacteroidota had similar potential glycan niches in the consumption of the main component of transparent exopolymer particles (sulfated fucose and rhamnose containing polysaccharide and sulfated-N-glycan), developing considerable niche overlap among these taxa. The most abundant CAZymes and transporter genes as well as the widest glycan niche in the abundant bacterial taxa implied their potential key roles on the organic carbon utilization, and the high degree of glycan niches separation and polysaccharide composition importantly influenced bacterial communities in the coastal waters of PRE. These findings expand the current understanding of the organic carbon biotransformation, underlying the size-fractionated glycan niche separation near the estuarine system.

Keywords: glycan niche; metagenomics analysis; microbial CAZyme diversity; microbiome; the Pearl River Estuary.