The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist

Garret Suen,Natalia N Ivanova,Colleen Drinkwater,Cameron R Currie,Jan Deneke,Lynne A Goodwin,Natalia Mikhailova,David Mead,Julie Boyum,Frank O Aylward,Paul J Weimer,Phillip J Brumm,Olga Chertkov,David M Stevenson,Wenjun Li

doi:10.1371/journal.pone.0018814

Abstract

Fibrobacter succinogenes is an important member of the rumen microbial community that converts plant biomass into nutrients usable by its host. This bacterium, which is also one of only two cultivated species in its phylum, is an efficient and prolific degrader of cellulose. Specifically, it has a particularly high activity against crystalline cellulose that requires close physical contact with this substrate. However, unlike other known cellulolytic microbes, it does not degrade cellulose using a cellulosome or by producing high extracellular titers of cellulase enzymes. To better understand the biology of F. succinogenes, we sequenced the genome of the type strain S85 to completion. A total of 3,085 open reading frames were predicted from its 3.84 Mbp genome. Analysis of sequences predicted to encode for carbohydrate-degrading enzymes revealed an unusually high number of genes that were classified into 49 different families of glycoside hydrolases, carbohydrate binding modules (CBMs), carbohydrate esterases, and polysaccharide lyases. Of the 31 identified cellulases, none contain CBMs in families 1, 2, and 3, typically associated with crystalline cellulose degradation. Polysaccharide hydrolysis and utilization assays showed that F. succinogenes was able to hydrolyze a number of polysaccharides, but could only utilize the hydrolytic products of cellulose. This suggests that F. succinogenes uses its array of hemicellulose-degrading enzymes to remove hemicelluloses to gain access to cellulose. This is reflected in its genome, as F. succinogenes lacks many of the genes necessary to transport and metabolize the hydrolytic products of non-cellulose polysaccharides. The F. succinogenes genome reveals a bacterium that specializes in cellulose as its sole energy source, and provides insight into a novel strategy for cellulose degradation.

Highlights

Herbivorous mammals are essential components of terrestrial ecosystems and are major participants in the global carbon cycle, as well as the foundation of animal agriculture
Phylogenetic placement of F. succinogenes F. succinogenes was originally placed within the phylum
If F. succinogenes is closely related to bacteria in a different phylum, it is expected that a majority of proteins in F. succinogenes would have close matches to proteins in bacteria belonging to that phylum

Summary

Introduction

Herbivorous mammals are essential components of terrestrial ecosystems and are major participants in the global carbon cycle, as well as the foundation of animal agriculture. Much of the plant biomass consumed by herbivores is degraded by symbiotic microorganisms in the host digestive tract. This symbiotic interaction between plant-degrading microbial communities and their herbivorous hosts is perhaps best exemplified by ruminants such as domestic cattle. The ruminal fermentation is characterized by an incomplete anaerobic digestion in which plant material is converted to a mixture of C2 to C6 volatile fatty acids (VFAs), some of which are produced via intermediates such as succinic and lactic acids. These VFAs are used by the host as its primary energy source. The ruminal microflora are responsible for producing other metabolic products, including methane, carbon dioxide and microbial cells, the last of which are digested postruminally to supply a major portion of the protein requirements of the host

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