Adaptive responses of Rhodococcus aetherivorans L13 to oligotrophy: genome and transcriptomic analysis

Abstract

The wide ecological distribution of actinobacteria suggests that they have developed efficient mechanisms to adapt to extremely nutritionally deficient (oligotrophic) conditions. The impact of nutrient limitation typically observed in oligotrophic areas on bacteria remains to be assessed for many species. The non-model Rhodococcus aetherivorans L13can grow under oligotrophic conditions, even without an added carbon source. Oligotrophic cells of L13 undergo physiologicaland morphological changes compared to glucose-grown cells, including forming short-fragmenting cells, producing an extracellular polymeric substance, and a 26-fold decrease in respiratory activity. We conducted genome sequencing of L13 and assembled the entire genome, subsequently comparing the abundance of gene transcripts in oligotrophic cells to those of glucose-grown cells, to explore the oligotrophy-responsive mechanisms at the genetic level. The genome comprises6,543,485 base pairs, distributed across a single chromosome and six extrachromosomal plasmids (one linear and five circular). RNA-Seq analysis revealed the significant dysregulation of 2,665 genes (44% of the total genes detected). Results suggested a profound reorganization of its carbon and energy metabolism, including the activation of (i) mechanisms for utilizing air components; (ii) various dehydrogenases involved in aldehyde and alcohol metabolism, (iii) several enzymesinvolved in C2 metabolism, glyoxylate shunt, and TCA bypass routes, and downregulation of several genes that encode CO2 releasing-decarboxylase enzymes. Our results suggested that the adaptation strategy of L13 to oligotrophic conditions is supported by a combination of metabolic events, including low metabolic activity, the activation of C2 and ketoacids metabolism, and the display of a carbon conservative metabolic program.