Azoarcus sp. CIB, an Anaerobic Biodegrader of Aromatic Compounds Shows an Endophytic Lifestyle

Abstract

BackgroundEndophytic bacteria that have plant growth promoting traits are of great interest in green biotechnology. The previous thought that the Azoarcus genus comprises bacteria that fit into one of two major eco-physiological groups, either free-living anaerobic biodegraders of aromatic compounds or obligate endophytes unable to degrade aromatics under anaerobic conditions, is revisited here.Methodology/Principal FindingsLight, confocal and electron microscopy reveal that Azoarcus sp. CIB, a facultative anaerobe β-proteobacterium able to degrade aromatic hydrocarbons under anoxic conditions, is also able to colonize the intercellular spaces of the rice roots. In addition, the strain CIB displays plant growth promoting traits such nitrogen fixation, uptake of insoluble phosphorus and production of indoleacetic acid. Therefore, this work demonstrates by the first time that a free-living bacterium able to degrade aromatic compounds under aerobic and anoxic conditions can share also an endophytic lifestyle. The phylogenetic analyses based on the 16S rDNA and nifH genes confirmed that obligate endophytes of the Azoarcus genus and facultative endophytes, such as Azoarcus sp. CIB, locate into different evolutionary branches.Conclusions/SignificanceThis is the first report of a bacterium, Azoarcus sp. CIB, able to degrade anaerobically a significant number of aromatic compounds, some of them of great environmental concern, and to colonize the rice as a facultative endophyte. Thus, Azoarcus sp. CIB becomes a suitable candidate for a more sustainable agricultural practice and phytoremediation technology.

Whole-genome analysis of Azoarcus sp. strain CIB provides genetic insights to its different lifestyles and predicts novel metabolic features

“…CIB is able to fix nitrogen as a diazotroph [16], which was confirmed through genome analyses by the presence of a nitrogen fixation regulon. Thus, a nif gene cluster encoding the synthesis and maturation of the nitrogenase required to fix nitrogen is closely linked to another cluster that likely encodes a RnfI membrane complex driving a reverse electron flow from NADH to reduce ferredoxin FdxN, which serves as the electron donor to nitrogenase [45].…”

“…Therefore, these data strongly suggest that strain CIB is indeed a bacterial species different to those sequenced so far. Taken into account previous phylogenetic analyses of the 16S rDNA sequence of strain CIB and that of the other Azoarcus species known so far [16,32], Azoarcus sp. CIB would be closely related to A. evansii/A.…”

“…CIB has also the ability to grow in association with plants, colonizing the intercellular spaces of the exodermis of rice roots. In addition, the strain CIB displays plant growth promoting traits such the ability to uptake insoluble phosphorous, production of indoleacetic acid (IAA) or nitrogen fixation [16]. Thus, Azoarcus sp.…”

“…Thus, Azoarcus sp. CIB may represent the prototype of a subgroup of Azoarcus strains that share the anaerobic biodegradation of aromatic hydrocarbons with a facultative endophytic lifestyle [16]. Since Azoarcus sp.…”

Degradation of cyclic diguanosine monophosphate by a hybrid two-component protein protects Azoarcus sp. strain CIB from toluene toxicity

“…Azoarcus sp. CIB has distinct oxygen-requiring aerobic and oxygen-sensitive anaerobic pathways for aromatic hydrocarbon degradation (4)(5)(6). Within the bss-bbs gene cluster responsible for the anaerobic degradation of toluene/m-xylene, there is a gene, tolR (AzCIB_4516), that has no orthologs in any of the homologous bss-bbs clusters described so far in other bacteria (4,6,7).…”