Characterization of Potential Polysaccharide Utilization Systems in the Marine Bacteroidetes Gramella Flava JLT2011 Using a Multi-Omics Approach.

Kai Tang,Nianzhi Jiao,Yingfan Lin,Yu Han

doi:10.3389/fmicb.2017.00220

Abstract

Members of phylum Bacteroidetes are distributed across diverse marine niches and Flavobacteria is often the predominant bacterial class decomposing algae-derived polysaccharides. Here, we report the complete genome of Gramella flava JLT2011 (Flavobacteria) isolated from surface water of the southeastern Pacific. A remarkable genomic feature is that the number of glycoside hydrolase (GH) genes in the genome of G. flava JLT2011 is more than 2-fold higher than that of other Gramella species. The functional profiles of the GHs suggest extensive variation in Gramella species. Growth experiments revealed that G. flava JLT2011 has the ability to utilize a wide range of polysaccharides for growth such as xylan and homogalacturonan in pectin. Nearly half of all GH genes were located on the multi-gene polysaccharide utilization loci (PUL) or PUL-like systems in G. flava JLT2011. This species was also found to harbor the two xylan PULs and a pectin PUL, respectively. Gene expression data indicated that more GHs and sugar-specific outer-membrane susC-susD systems were found in the presence of xylan than in the presence of pectin, suggesting a different strategy for heteropolymeric xylan and homoglacturonan utilization. Multi-omics data (transcriptomics, proteomics, and metabolomics) indicated that xylan PULs and pectin PUL are respectively involved in the catabolism of their corresponding polysaccharides. This work presents a comparison of polysaccharide decomposition within a genus and expands current knowledge on the diversity and function of PULs in marine Bacteroidetes, thereby deepening our understanding of their ecological role in polysaccharide remineralization in the marine system.

Highlights

Members of the Bacteroidetes, formerly known as the Cytophaga-Flavobacteria-Bacteroides phylum, are diverse and widely distributed in marine ecosystems (Glöckner et al, 1999; Kirchman, 2002; Alonso et al, 2007)
Polysaccharides Utilization Systems in Marine Bacteroidetes substances as carbon and energy sources (Bauer et al, 2006; McBride et al, 2009; Qin et al, 2010; Mann et al, 2013). These bacteria use their wide array of peptidases and carbohydrateactive enzymes (CAZymes), including glycoside hydrolases (GHs), carbohydrate esterases (CEs), polysaccharide lyases (PLs), and glycoside transferases (GTs) to efficiently degrade polymers such as proteins and polysaccharides (Bauer et al, 2006; Fernández-Gómez et al, 2013)
The genome contains 184 genes encoding CAZymes, which is significantly higher than that of other Gramella species (G. forsetii KT0803, 118; G. echinicola DSM19838, 108; G. portivictoriae DSM23547, 119; Table S2). It harbors 96 genes that encode GHs that represent 34 CAZyme superfamilies (Table S3), compared to G. forsetii KT0803 that has 42 GHs genes that were assigned to 20 superfamilies (Table S2)

Summary

Introduction

Members of the Bacteroidetes, formerly known as the Cytophaga-Flavobacteria-Bacteroides phylum, are diverse and widely distributed in marine ecosystems (Glöckner et al, 1999; Kirchman, 2002; Alonso et al, 2007). The optimal BLASTP hits of approximately two-thirds of the GHs of G. flava JLT2011 were aligned with non-Gramella bacterial species, of which most were homologous to those of bacteria from class Flavobacteria of phylum Bacteroidetes such as Zunongwangia profunda SM-A87 (Table S3, Figure S2). The G. flava JLT2011 genome appears to have a high frequency of GHs (>20 genes per Mbp), which is similar to other Bacteroidetes, including Z. profunda SMA87 from deep-sea sediments (Qin et al, 2010), Echinicola vietnamensis DSM17526 from a lagoon of Nha Trang Bay, South China Sea (Nedashkovskaya et al, 2007), and Leeuwenhoekiella blandensis MED217 from the open ocean (Pinhassi et al, 2006; Figure 2A).

Results

Conclusion