Journal Article

Nonspecific Binding of a Putative S-Layer Protein to Plant Cell Wall Polysaccharides-Implication for Growth Competence of Lactobacillus brevis in the Gut Microbiota

Luo, Huiying, Yang, Daoxin, Guo, Kairui, Su, Xiaoyun, Huang, Huoqing, Wang, Yuan, Hao, Zhenzhen, Ge, Jianzhong, Zhang, Wenjing

2025

Overview

Plant cell wall polysaccharides (PCWPs) serve as an abundant but recalcitrant carbon source for many microbes living in the gut of humans and animals. An adhesion to PCWPs is common in gut bacteria and can even be observed in the lactobacilli, which are supposed to promote the growth competence of these non-PCWP degraders because of the facilitated acquisition of newly released oligosaccharides. Nevertheless, the binding of molecules of lactobacilli to PCWPs and the underlying mechanisms remain largely unknown. By analyzing the transcriptome of grown in xylan supplemented with a xylanase, a gene was identified to encode a putative S-layer PCWP-binding protein (Lb1145). Lb1145 was predicted to have four domains, among which domains 1 and 2 were responsible for binding PCWPs. The binding was nonspecific, since structurally distinct PCWPs, e.g., cellulose, xylan, mannan, and chitin, and even lignin, were all bound by Lb1145. Both of the two N-terminal domains have a high pI, and we demonstrated that a non-enzymatic glycosylation-like process plays an important role in binding. Compared with another surface protein, i.e., the WxL protein Lb630, Lb1145 displayed a binding preference for the phloem sieve tube in the wheat stem section. Moreover, Lb1145 could bind ten strains within the , , , and genera among the seventeen selected gut bacterial species. An analysis of the reported S-layer proteins from the Gram-positive bacteria (lactobacilli and bifidobacteria) and outer membrane proteins from the Gram-negative ( and ) indicated that bacterial cell surface proteins with high pI values are not rare. The high pI-based and non-enzymatic glycosylation-like process-mediated binding represents a new paradigm and may be popular in gut bacterial surface proteins binding to PCWPs, with important physiological implications in growth competition in the gut microbiota.

• Publisher: MDPI AG,Multidisciplinary Digital Publishing Institute (MDPI)
• Subject: Amino acids / Bacteria / Bacterial Adhesion / Bacterial Proteins - genetics / Bacterial Proteins - metabolism / Carbon / Cell Wall - metabolism / Cellulose / Gastrointestinal Microbiome / Gut microbiota / Levilactobacillus brevis - genetics / Levilactobacillus brevis - growth & development / Levilactobacillus brevis - metabolism / Membrane Glycoproteins - chemistry / Membrane Glycoproteins - genetics / Membrane Glycoproteins - metabolism / Plant Cells - metabolism / Polysaccharides - metabolism / Probiotics / Protein Binding / Proteins