Diverse Horizontally Transferred Cellulose Biosynthesis Gene Clusters in Escherichia coli Strains.

The phosphoethanolamine-modified exopolysaccharide cellulose synthesized by the type IIa cellulose biosynthesis nanomachine is a major extracellular matrix component of Escherichia coli. Here, we aim to investigate whether homologs of bcsABC genes of the core genome EcType 1 bcs cellulose biosynthesis gene cluster, which are diminished or abolished in high-virulence isolates, and entire clusters are mobilized on plasmids and occasionally manifested on E. coli chromosomes at alternative locations. While EcType BcsA2 and BcsA3 cellulose synthases are restricted to the genus Escherichia, the EcType BcsA4 cellulose synthase and associated bcs gene products are highly similar to Klebsiella pneumoniae counterparts. Cyclic di-GMP turnover proteins not previously recognized to post-translationally regulate cellulose biosynthesis on the chromosomal level are frequently co-localized with novel bcs genes. Thermotolerant meat-derived E. coli 730V1 uniquely harbors an EcType 4 bcs gene cluster of type Ib with a type IIb bcsG gene on a plasmid. Chemical, phenotypic and genetic evidence showed cellulose biosynthesis, cellulose-dependent cell aggregation and activation of biosynthesis by the second messenger cyclic di-GMP, an allosteric activator of the cellulose synthase. With gene duplication, horizontal gene transfer and recombination to contribute to the multiplication and diversification of bcs gene clusters in a number of different bacterial species, the extent and ecological role(s) of the multiplication, transfer and replacement of cellulose biosynthesis gene clusters, as well as in species other than E. coli, still need to be unraveled. Our data indicate, however, that although diversification and multiplication of bcs clusters is ongoing in the species E. coli, these events become rarely manifested in the population.