Structure and Evolution of Glycogen Branching Enzyme N-Termini From Bacteria.

Liang Wang,Qinghua Liu,Xiuqing Chen,Michael J. Wise,Xiang Wu,Jianye Yang,Daoquan Tang,Junfeng Hu,Chao Ma,James Asenso

doi:10.3389/fmicb.2018.03354

Liang Wang, Qinghua Liu + Show 8 more

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https://doi.org/10.3389/fmicb.2018.03354

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Abstract

In bacteria, glycogen plays important roles in carbon and energy storage. Its structure has recently been linked with bacterial environmental durability. Among the essential genes for bacterial glycogen metabolism, the glgB-encoded branching enzyme GBE plays an essential role in forming α-1,6-glycosidic branching points, and determines the unique branching patterns in glycogen. Previously, evolutionary analysis of a small sets of GBEs based on their N-terminal domain organization revealed that two types of GBEs might exist: (1) Type 1 GBE with both N1 and N2 (also known as CBM48) domains and (2) Type 2 GBE with only the N2 domain. In this study, we initially analyzed N-terminal domains of 169 manually reviewed bacterial GBEs based on hidden Markov models. A previously unreported group of GBEs (Type 3) with around 100 amino acids ahead of the N1 domains was identified. Phylogenetic analysis found clustered patterns of GBE types in certain bacterial phyla, with the shorter, Type 2 GBEs predominantly found in Gram-positive species, while the longer Type 1 GBEs are found in Gram-negative species. Several in vitro studies have linked N1 domain with transfer of short oligosaccharide chains during glycogen formation, which could lead to small and compact glycogen structures. Compact glycogen degrades more slowly and, as a result, may serve as a durable energy reserve, contributing to the enhanced environmental persistence for bacteria. We were therefore interested in classifying GBEs based on their N-terminal domain via large-scale sequence analysis. In addition, we set to understand the evolutionary patterns of different GBEs through phylogenetic analysis at species and sequence levels. Three-dimensional modeling of GBE N-termini was also performed for structural comparisons. A further study of 9,387 GBE sequences identified 147 GBEs that might belong to a possibly novel group of Type 3 GBE, most of which fall into the phylum of Actinobacteria. We also attempted to correlate glycogen average chain length (ACL) with GBE types. However, no significant conclusions were drawn due to limited data availability. In sum, our study systematically investigated bacterial GBEs in terms of domain organizations from evolutionary point of view, which provides guidance for further experimental study of GBE N-terminal functions in glycogen structure and bacterial physiology.

Highlights

Glycogen is a widespread water-soluble homogeneous polysaccharide with α-1,4-glycosidic bonds in linear chains and α-1,6-glycosidic linkages at the branching points (Wang and Wise, 2011)
As for Actinobacteria, GBE in a single species Rubrobacter xylanophilus is more related with Proteobacteria phylum at sequence level while all other GBEs in Actinobacteria are grouped together
Since GBE N-terminus can be divided into distinct groups, we investigated the relationships between GBE types and average chain length (ACL) of bacterial glycogen through literature mining and correlation analysis

Summary

Introduction

Glycogen is a widespread water-soluble homogeneous polysaccharide with α-1,4-glycosidic bonds in linear chains and α-1,6-glycosidic linkages at the branching points (Wang and Wise, 2011). The uniquely branched structure of glycogen in bacteria is normally due to a group of coordinated enzymes: ADP-glucose pyrophosphorylase (GlgC), glycogen synthase (GlgA), glycogen branching enzyme (GlgB or GBE), glycogen phosphorylase (GlgP), and glycogen debranching enzyme (GlgX) (Wilson et al, 2010; Wang and Wise, 2011). GlgC, GlgA, and GBE are involved in glycogen synthesis processes, while GlgP and GlgX function as degradation enzymes (Wang and Wise, 2011). Take GBE in E. coli for example. α-1,4-glycosidic bonds in linear chains are broken first and short oligosaccharides no less six glucosyl residues, with eight or more glucosyl residues preferred, are transferred to neighboring or the same chains to form α-1,6-glycosidic bonds linked branches (Binderup et al, 2000; Wang et al, 2015)

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