Butyrivibrio hungateiMB2003 competes effectively for soluble sugars released byButyrivibrio proteoclasticusB316Tfrom growth on xylan or pectin

Abstract

ABSTRACT Rumen bacterial species belonging to the genera Butyrivibrio are important degraders of plant polysaccharides, particularly hemicelluloses (arabinoxylans) and pectin. Currently, four distinct species are recognized which have very similar substrate utilization profiles, but little is known about how these microorganisms are able to co-exist in the rumen. To investigate this question, Butyrivibrio hungatei (MB2003) and Butyrivibrio proteoclasticus (B316 T ) were grown alone or in co-culture on the insoluble substrates, xylan or pectin, and their growth, release of sugars, fermentation end products and transcriptomes were examined. In single cultures, B316 T was able to degrade and grow well on xylan and pectin, while B. hungatei MB2003 was unable to utilize either of these insoluble substrates to support significant growth. Co-cultures of B316 T grown with MB2003 revealed that MB2003 showed almost equivalent growth to B316 T when either xylan or pectin were supplied as substrates. The effect of co-culture on the transcriptomes of B316 T and MB2003 was very marked; B316 T transcription was largely unaffected by the presence MB2003, but MB2003 expressed a wide range of genes encoding carbohydrate degradation/metabolism and oligosaccharide transport/assimilation in order to compete with B316 T for the released sugars. These results suggest that B316 T has a role as an initiator of the primary solubilization of xylan and pectin, while MB2003 competes effectively as a scavenger for the released soluble sugars to enable its growth and maintenance in the rumen. IMPORTANCE Feeding a global population of nine billion people and climate change are the primary challenges facing agriculture today. Determining the roles of rumen microbes involved in plant polysaccharide breakdown is fundamental to understanding digestion and maximizing productivity of ruminant livestock. Butyrivibrio are abundant rumen bacteria and are a substantial source of polysaccharide-degrading enzymes with biotechnological applications for the depolymerization of lignocellulosic material. Our findings suggest that closely related species of Butyrivibrio have developed unique strategies for the degradation of plant fibre and the subsequent assimilation of carbohydrates in order to coexist in the competitive rumen environment. The identification of genes related to their enzymatic machinery by which these bacteria work in concert to degrade these different forms of polysaccharides contributes to our understanding of carbon flow in the rumen.