The Role of Two Linear β-Glucans Activated by c-di-GMP in Rhizobium etli CFN42

Abstract

Bacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan, cellulose, and the new described Mixed Linkage β-Glucan (MLG). Bis-(3′,5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a universal bacterial second messenger that usually promote EPS production. Here, we report Rhizobium etli as the first bacterium capable of producing cellulose and MLG. Significant amounts of these two β-glucans are not produced under free-living laboratory conditions, but their production is triggered upon elevation of intracellular c-di-GMP levels, both contributing to Congo red (CR+) and Calcofluor (CF+) phenotypes. Cellulose turned out to be more relevant for free-living phenotypes promoting flocculation and biofilm formation under high c-di-GMP conditions. None of these two EPS are essential for attachment to roots of Phaseolus vulgaris, neither for nodulation nor for symbiotic nitrogen fixation. However, both β-glucans separately contribute to the fitness of interaction between R. etli and its host. Overproduction of these β-glucans, particularly cellulose, appears detrimental for symbiosis. This indicates that their activation by c-di-GMP must be strictly regulated in time and space and should be controlled by different, yet unknown, regulatory pathways.

Multifaceted properties of TiO2 nanoparticles synthesized using Mangifera indica and Azadirachta indica plant extracts: antimicrobial, antioxidant, and non-linear optical activity investigation for sustainable agricultural applications

“…Most glucan polymers are composed of glucose units linked by 1,3 linkages (65–90%), although there are variations with β-1,6, β-1,4, α-1,3, and α-1,4 linkages depending on the fungal species. 86 The β-1,3- d -glucan and chitin molecules form intrachain hydrogen bonds and can assemble into fibrous microfibrils, creating a basket-like scaffold around the cell. 87 β-1,3- d -glucan is responsible for covalently linking other components, making it the critical structural component of the cell wall.…”

Exopolysaccharides Producing Bacteria: A Review

“…Information is exchanged using specialized chemical signaling molecules, through which the microbial community acts as a single organism [142]. Cyclic diguanylate (c-di-GMP) is an intracellular signaling molecule that regulates the transition from a planktonic state in the environment to a surface-associated biofilm for many bacteria including Agrobacterium sp., Rhizobium sp., Salmonella sp., Vibrio sp., Pseudomonas sp., and others [80,84,140,143]. The review by Augimeri et al (2015) highlighted the diversity of BC biosynthesis and regulation and its role in environmental interactions by discussing diverse biofilm-producing Proteobacteria [136].…”

“…BC is produced by Gram-negative bacteria of the genera Komagataeibacter ( Gluconacetobacter ) [ 76 , 77 ], Acetobacter [ 78 ], Gluconobacter [ 79 ], Agrobacterium [ 80 ], Achromobacter [ 81 ], Enterobacter [ 82 , 83 ], Rhizobium [ 84 ], Pseudomonas [ 85 ], Salmonella [ 86 ], and others, as well as Gram-positive bacteria of the genera Bacillus [ 87 ], Sarcina , and Rhodococcus [ 88 ]. The most common and highly productive BC producers are acetic bacteria species of the Komagataeibacter genus such as K. xylinus and K. hansenii .…”

“…And in this case, BC serves as a kind of molecular glue to ensure interactions in nature [ 136 ]. For example, BC is involved in the adhesion of bacterial cells of the genus Rhizobium during symbiosis with leguminous plants, Agrobacterium and Salmonella in infection, contributing to the colonization of plants providing protection against competitors [ 35 , 84 , 86 ]. Cellulose and its derivatives are important components of biofilms and play a significant role in regulating the virulence of plant and human pathogens [ 32 , 137 , 138 ].…”