Microbial Encounters of a Symbiotic Kind: Attaching to Roots and Other Surfaces

Abstract

Attachment of bacteria to plant surfaces is a necessary prelude to the interaction, either pathological or mutualistic, that follows. For symbiotic nitrogen fixation to occur and, in particular, for nodules to develop for housing the nitrogen-fixing bacteria in the legume–Rhizobium mutualism, attachment of rhizobia to roots is critical. Nodules form on some legume roots as a consequence of Nod factor perception if the rhizobia do not attach, but they remain uninfected because attachment is needed for infection-thread formation. Numerous studies have shown that rhizobial cell surface components are required for optimal root attachment and colonization. These components include polysaccharides such as exopolysaccharides, lipopolysaccharides, cyclic β-1,2-glucans, and cellulose fibrils; and also proteins, including flagellae, pili, rhicadhesin, and a bacterial lectin known as Bj38. Loss of function of genes encoding exo-, capsular-, and lipopolysacchrides as well as cyclic β-1,2-glucan often result in diminished root attachment and poorly infected nodules. However, no mutant phenotypes have been described for the loss of function of either rhicadhesin or bacterial lectin because genes encoding these traits have not yet been identified. Rhizobium leguminosarum mutants defective in cellulose fibril production still induce nitrogen-fixing nodule formation, and moreover, not all rhizobia synthesize cellulose fibrils, strongly suggesting that fibrils are not universally required for attachment to plant roots. On the plant side, very little is known about the factors required for rhizobial attachment. Carbohydrate-binding proteins, particularly lectins, have been implicated, but few other plant proteins have been described. This review describes what is known about the genes and proteins that are involved in attachment and colonization of rhizobia on legumes. We focus not only on attachment to root hairs and epidermal cells, but also on ex planta adherence. To that end, we consider rhizobial attachment to the root surface as well as to abiotic surfaces as a biofilm, i.e., a structured community of bacteria adherent to a surface and to each other, and surrounded by exopolymer. We also examine the effects of cell surface mutations on biofilm development in other bacteria with the goal of establishing commonalities with nitrogen-fixing rhizobia.