Extrachromosomal, extraordinary and essential—the plasmids of the Roseobacter clade

Abstract

The alphaproteobacterial Roseobacter clade (Rhodobacterales) is one of the most important global players in carbon and sulfur cycles of marine ecosystems. The remarkable metabolic versatility of this bacterial lineage provides access to diverse habitats and correlates with a multitude of extrachromosomal elements. Four non-homologous replication systems and additional subsets of individual compatibility groups ensure the stable maintenance of up to a dozen replicons representing up to one third of the bacterial genome. This complexity presents the challenge of successful partitioning of all low copy number replicons. Based on the phenomenon of plasmid incompatibility, we developed molecular tools for target-oriented plasmid curing and could generate customized mutants lacking hundreds of genes. This approach allows one to analyze the relevance of specific replicons including so-called chromids that are known as lifestyle determinants of bacteria. Chromids are extrachromosomal elements with a chromosome-like genetic imprint (codon usage, GC content) that are essential for competitive survival in the natural habitat, whereas classical dispensable plasmids exhibit a deviating codon usage and typically contain type IV secretion systems for conjugation. The impact of horizontal plasmid transfer is exemplified by the scattered occurrence of the characteristic aerobic anoxygenic photosynthesis among the Roseobacter clade and the recently reported transfer of the 45-kb photosynthesis gene cluster to extrachromosomal elements. Conjugative transmission may be the crucial driving force for rapid adaptations and hence the ecological prosperousness of this lineage of pink bacteria.

Molecular and phenotypic analyses reveal the non-identity of the Phaeobacter gallaeciensis type strain deposits CIP 105210T and DSM 17395

“…The same explanation is supported by the presence of a type IV secretion system on the fourth 86 kb plasmid of the P. inhibens type strain DSM 16374 T (Dogs, M. and others, unpublished), which may be responsible for plasmid mobilization via conjugation (Petersen et al, 2013). In the near future, genome sequencing and comparative genomics of more distantly related strains, such as Phaeobacter arcticus, will help to reveal the extent of horizontal exchange and vertical evolution within the Roseobacter clade.…”

Evolutionary Ecology of the Marine Roseobacter Clade

“…The taxonomic distribution of these chemolithotrophic gene sets does not map coherently to species phylogeny, suggesting that gain and loss of these traits have occurred multiple times during Roseobacter evolution, consistent with the scenario that roseobacters have continuously explored new ecological habitats. A few of these ecologically relevant genetic traits, including complete photosynthetic gene clusters (58), capabilities for production of the antibiotic tropodithietic acid (TDA) (59,60), and type IV secretion systems (61), are found on plasmids, suggesting that extrachromosomal DNA could be an important mechanism by which genes useful for environmental adaptation are transferred among roseobacters.…”

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…Furthermore, plasmids, chromids, and other extrachromosomal mobile genetic elements, such as the phagelike gene transfer agents (GTAs), are common in MRC bacteria, contributing to gene transfer, metabolic versatility, and fitness, especially in microhabitats such as those on surfaces and in biofilms (762,(786)(787)(788)(789). In some MRC bacteria, the genes encoding the biosynthesis of TDA, siderophores, and extracellular polysaccharides are located on plasmids or chromids, indicating the direct involvement of extrachromosomal genetic material in bacterial surface associations (603,789). For example, Marinovum algicola DG898 harbors three plasmids and eight chromids, and one of the chromids harbors the 52-kb biofilm functional gene cluster that is essential for surface attachment and adaptation to the phycosphere (790).…”