TY - JOUR
T1 - Outer membrane vesicles from Fibrobacter succinogenes S85 contain an array of carbohydrate-active enzymes with versatile polysaccharide-degrading capacity
AU - Arntzen, Magnus
AU - Várnai, Anikó
AU - Mackie, Roderick I.
AU - Eijsink, Vincent G.H.
AU - Pope, Phillip B.
N1 - Funding Information:
The authors would like to thank Dr. Roger Scherrers at Wyatt (Dernbach, Germany) for analysis of vesicles using dynamic light scattering and Dr. Bj?rge Westereng (NMBU, Norway) for helpful discussions. The imaging was performed at the Imaging Centre Campus ?s, Department of Plant Sciences, NMBU, Norway. The proteomics data has been deposited to the ProteomeXchange consortium (http://proteomecentral.proteomexchange.org) via the PRIDE partner repository (Vizcaino et al.,) with the dataset identifier PXD005442.
PY - 2017/7
Y1 - 2017/7
N2 - Fibrobacter succinogenes is an anaerobic bacterium naturally colonising the rumen and cecum of herbivores where it utilizes an enigmatic mechanism to deconstruct cellulose into cellobiose and glucose, which serve as carbon sources for growth. Here, we illustrate that outer membrane vesicles (OMVs) released by F. succinogenes are enriched with carbohydrate-active enzymes and that intact OMVs were able to depolymerize a broad range of linear and branched hemicelluloses and pectin, despite the inability of F. succinogenes to utilize non-cellulosic (pentose) sugars for growth. We hypothesize that the degradative versatility of F. succinogenes OMVs is used to prime hydrolysis by destabilising the tight networks of polysaccharides intertwining cellulose in the plant cell wall, thus increasing accessibility of the target substrate for the host cell. This is supported by observations that OMV-pretreatment of the natural complex substrate switchgrass increased the catalytic efficiency of a commercial cellulose-degrading enzyme cocktail by 2.4-fold. We also show that the OMVs contain a putative multiprotein complex, including the fibro-slime protein previously found to be important in binding to crystalline cellulose. We hypothesize that this complex has a function in plant cell wall degradation, either by catalysing polysaccharide degradation itself, or by targeting the vesicles to plant biomass.
AB - Fibrobacter succinogenes is an anaerobic bacterium naturally colonising the rumen and cecum of herbivores where it utilizes an enigmatic mechanism to deconstruct cellulose into cellobiose and glucose, which serve as carbon sources for growth. Here, we illustrate that outer membrane vesicles (OMVs) released by F. succinogenes are enriched with carbohydrate-active enzymes and that intact OMVs were able to depolymerize a broad range of linear and branched hemicelluloses and pectin, despite the inability of F. succinogenes to utilize non-cellulosic (pentose) sugars for growth. We hypothesize that the degradative versatility of F. succinogenes OMVs is used to prime hydrolysis by destabilising the tight networks of polysaccharides intertwining cellulose in the plant cell wall, thus increasing accessibility of the target substrate for the host cell. This is supported by observations that OMV-pretreatment of the natural complex substrate switchgrass increased the catalytic efficiency of a commercial cellulose-degrading enzyme cocktail by 2.4-fold. We also show that the OMVs contain a putative multiprotein complex, including the fibro-slime protein previously found to be important in binding to crystalline cellulose. We hypothesize that this complex has a function in plant cell wall degradation, either by catalysing polysaccharide degradation itself, or by targeting the vesicles to plant biomass.
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U2 - 10.1111/1462-2920.13770
DO - 10.1111/1462-2920.13770
M3 - Article
C2 - 28447389
AN - SCOPUS:85019770530
VL - 19
SP - 2701
EP - 2714
JO - Environmental Microbiology
JF - Environmental Microbiology
SN - 1462-2912
IS - 7
ER -