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

Abstract

The genomic features of Azoarcus sp. CIB reflect its most distinguishing phenotypes as a diazotroph, facultative anaerobe, capable of degrading either aerobically and/or anaerobically a wide range of aromatic compounds, including some toxic hydrocarbons such as toluene and m-xylene, as well as its endophytic lifestyle. The analyses of its genome have expanded the catabolic potential of strain CIB toward common natural compounds, such as certain diterpenes, that were not anticipated as carbon sources. The high number of predicted solvent efflux pumps and heavy metal resistance gene clusters has provided the first evidence for two environmentally relevant features of this bacterium that remained unknown. Genome mining has revealed several gene clusters likely involved in the endophytic lifestyle of strain CIB, opening the door to the molecular characterization of some plant growth promoting traits. Horizontal gene transfer and mobile genetic elements appear to have played a major role as a mechanism of adaptation of this bacterium to different lifestyles. This work paves the way for a systems biology-based understanding of the abilities of Azoarcus sp. CIB to integrate aerobic and anaerobic metabolism of aromatic compounds, tolerate stress conditions, and interact with plants as an endophyte of great potential for phytostimulation and phytoremediation strategies. Comparative genomics provides an Azoarcus pan genome that confirms the global metabolic flexibility of this genus, and suggests that its phylogeny should be revisited.

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

“…TolR mediates its protective response to toluene only when Azoarcus sp. CIB is grown anaerobically, which agrees with the fact that the tolR gene is located within the bss-bbs cluster responsible for anaerobic degradation of toluene (6). Moreover, when expressed heterologously in P. aeruginosa, TolR responds to toluene to degrade c-di-GMP only under anaerobic conditions (SI Appendix, Fig.…”

“…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). The predicted TolR protein is a hybrid two-component system (HTCS) that includes sensor kinase (SK) and response regulator (RR) domains, an N-terminal Per-Arnt-Sim (PAS) domain, and a C-terminal EAL domain.…”

The ecology of anaerobic degraders of BTEX hydrocarbons in aquifers

“…2004; Martín-Moldes et al. 2015). For a facultative anaerobic degrader population established at the fringe of a BTEX plume, it would be advantageous to utilise either aerobic or anaerobic catabolism depending on oxygen availability.…”

The oil‐contaminated soil diazotroph Azoarcus oleariusDQS‐4T is genetically and phenotypically similar to the model grass endophyte Azoarcus sp. BH72

“…Subsequent to the discovery of the plant‐associated Azoarcus spp., new species were isolated from non‐plant sources, particularly from soil and/or water contaminated with aromatic compounds, such as A. anaerobius , A. evansii , A. taiwanensis , A. tolulyticus , A. toluvorans , A. toluclasticus and A. buckelii (Anders et al ., ; Zhou et al ., ; Springer et al ., ; Song et al ., ; Mechichi et al ., ; Lee et al ., ), as well as several strains that have not yet been described to species level (Rabus et al ., ; Nishizawa et al ., ; Fernández et al, ; Junghare et al ., ). These are taxonomically separate from the plant‐associated species (Reinhold‐Hurek and Hurek, ; Rabus et al ., ; Chen et al ., ; Fernández et al, ), and, in keeping with their habitats, also have a higher capacity to metabolize and degrade aromatic compounds, many of them under strict anaerobiosis, and, hence, may have biotechnological potential as agents for the remediation of oil‐polluted soils (Hurek and Reinhold‐Hurek, ; Martín‐Moldes et al, ). Both groups contain diazotrophs, but diazotrophy is not so common in the non‐plant‐associated group, and the nif genes of the two groups are not related (Hurek et al ., ; Fernández et al, ; Martín‐Moldes et al, ).…”

“…These are taxonomically separate from the plant‐associated species (Reinhold‐Hurek and Hurek, ; Rabus et al ., ; Chen et al ., ; Fernández et al, ), and, in keeping with their habitats, also have a higher capacity to metabolize and degrade aromatic compounds, many of them under strict anaerobiosis, and, hence, may have biotechnological potential as agents for the remediation of oil‐polluted soils (Hurek and Reinhold‐Hurek, ; Martín‐Moldes et al, ). Both groups contain diazotrophs, but diazotrophy is not so common in the non‐plant‐associated group, and the nif genes of the two groups are not related (Hurek et al ., ; Fernández et al, ; Martín‐Moldes et al, ). Indeed, so different are these two groups phylogenetically and phenotypically that there have been proposals to separate them into two genera (Reinhold‐Hurek and Hurek, ; Rabus et al ., ; Martín‐Moldes et al, ).…”