A metabolic switch is involved in lifestyle decisions in Photorhabdus luminescens

Abstract

SummaryPhotorhabdus luminescens is a species of Gramnegative bacteria that is pathogenic to insects while also maintaining a mutualistic association with nematodes from the family Heterorhabditis. P. luminescens elaborates an extensive secondary metabolism during the post-exponential phase of growth that includes the production of an antibiotic called 3-5-dihydroxy-4-isopropylstilbene (ST), an anthraquinone pigment (AQ) and bioluminescence. In this study we identified a mutant that was unable to produce ST, AQ and light. This mutation was found to be in the mdh gene, encoding malate dehydrogenase, a key enzyme in the tricarboxylic acid (TCA) cycle. Interestingly the mdh mutant was unaffected in virulence but was unable to support nematode growth and development in vivo or in vitro. This clearly establishes that secondary metabolism in P. luminescens is required for the mutualistic interaction with the nematode. Furthermore, the construction of mutations in key genes in other central metabolic pathways confirmed the critical role for the TCA cycle in both secondary metabolism and mutualism, but not in virulence. Therefore, we conclude that the TCA cycle is required for the transition of P. luminescens from pathogen to mutualist implicating the involvement of a metabolic switch in the regulation of lifestyle decisions in this bacterium.

Involvement of Vitamin B6Biosynthesis Pathways in the Insecticidal Activity of Photorhabdus luminescens

“…In the present study, the pdxB gene mutant lacks de novo vitamin B 6 synthesis, causing growthand pigmentation-deficient phenotypes under nutrient-poor conditions that are suppressed by nutrient-rich conditions and PLP supplementation. P. luminescens produces some secondary metabolites such as toxins and pigments during post-log-phase to stationary-phase growth (35,36). In addition, recent research revealed that the group-coordinated behavior of Photorhabdus, which includes pathogenicity, is controlled by density-dependent cell-cell communication (37)(38)(39).…”

Proteomic Investigation of Photorhabdus Bacteria for Nematode-Host Specificity

“…bioluminescence, an anthraquinone pigment (AQ) and an antibiotic 3-5-dihydroxy-4-isopropylstilbene), and might affect host specificity and symbiosis indirectly. For e.g., Plu4547 (mdh) was previously identified to be involved in symbiosis between Photorhabdus and Heterorhabditis [14]. mdh encodes for malate dehydrogenase which is a key tricarboxylic acid (TCA) cycle enzyme.…”

“…mdh encodes for malate dehydrogenase which is a key tricarboxylic acid (TCA) cycle enzyme. It was observed that nematode growth and development was not supported by an mdh mutant, establishing the role for secondary metabolism in bacteria-nematode symbiotic interactions [14]. Similarly, an alarmone (p)ppGpp is needed for the symbiont bacteria P. luminescens to sustain nematode development and growth through its effect on secondary metabolism.…”

“…Recently, the details of symbiont colonization sites in the nematode gut, and the developmental progression of this symbiotic relationship has been elucidated for PhotorhabdusHeterorhabditis pair [12]. Some of the bacterial genes and processes necessary for symbiotic colonization of the nematodes have also been identified [13][14][15][16].…”

Mass Production of the Beneficial Nematode Heterorhabditis bacteriophora and Its Bacterial Symbiont Photorhabdus luminescens

“…This process produces primary and secondary forms (phase I and phase II) which differ morphologically and physiologically [39][40][41] such as the association of coccoid bodies with phase I cells (Fig. 6).…”