R-type bacteriocins of Xenorhabdus bovienii determine the outcome of interspecies competition in a natural host environment

Abstract

Xenorhabdus species are bacterial symbionts of Steinernema nematodes and pathogens of susceptible insects. Different species of Steinernema nematodes carrying specific species of Xenorhabdus can invade the same insect, thereby setting up competition for nutrients within the insect environment. While Xenorhabdus species produce both diverse antibiotic compounds and prophage-derived R-type bacteriocins (xenorhabdicins), the functions of these molecules during competition in a host are not well understood. Xenorhabdus bovienii (Xb-Sj), the symbiont of Steinernema jollieti, possesses a remnant P2-like phage tail cluster, xbp1, that encodes genes for xenorhabdicin production. We show that inactivation of either tail sheath (xbpS1) or tail fibre (xbpH1) genes eliminated xenorhabdicin production. Preparations of Xb-Sj xenorhabdicin displayed a narrow spectrum of activity towards other Xenorhabdus and Photorhabdus species. One species, Xenorhabdus szentirmaii (Xsz-Sr), was highly sensitive to Xb-Sj xenorhabdicin but did not produce xenorhabdicin that was active against Xb-Sj. Instead, Xsz-Sr produced high-level antibiotic activity against Xb-Sj when grown in complex medium and lower levels when grown in defined medium (Grace’s medium). Conversely, Xb-Sj did not produce detectable levels of antibiotic activity against Xsz-Sr. To study the relative contributions of Xb-Sj xenorhabdicin and Xsz-Sr antibiotics in interspecies competition in which the respective Xenorhabdus species produce antagonistic activities against each other, we co-inoculated cultures with both Xenorhabdus species. In both types of media Xsz-Sr outcompeted Xb-Sj, suggesting that antibiotics produced by Xsz-Sr determined the outcome of the competition. In contrast, Xb-Sj outcompeted Xsz-Sr in competitions performed by co-injection in the insect Manduca sexta, while in competition with the xenorhabdicin-deficient strain (Xb-Sj:S1), Xsz-Sr was dominant. Thus, xenorhabdicin was required for Xb-Sj to outcompete Xsz-Sr in a natural host environment. These results highlight the importance of studying the role of antagonistic compounds under natural biological conditions.

Ribosomally synthesized peptides, foreground players in microbial interactions: recent developments and unanswered questions

“…The Xenorhabdus specie s produce an arsenal of toxins and antimicrobials, including xenorhabdicin, which is a bacteriocin of the phage-tail type. 217 When nematodes compete within the insect, those carrying symbionts more successfully reproduce, presumably due to the inhibition of the symbiont competitors. Xenorhabdicin was shown to be required for Xenorhabdus to outcompete a Xenorhabdus strain sensitive to, but not producing xenorhabdicin in a natural host environment.…”

“…Xenorhabdicin was shown to be required for Xenorhabdus to outcompete a Xenorhabdus strain sensitive to, but not producing xenorhabdicin in a natural host environment. 217 A symbiont-mediated trade-off in host fitness across competitive contexts was established, since the costs of bacteriocin production make inhibitory strains with lower fitness than non-inhibitory ones in the absence of competition. 218 These results are in line with the rock-paper-scissors theory that was first proposed in vitro and in vivo for colicins, the proteinaceous bacteriocins produced by Escherichia coli .…”

Type Strains of Entomopathogenic Nematode-Symbiotic Bacterium Species, Xenorhabdus szentirmaii (EMC) and X. budapestensis (EMA), Are Exceptional Sources of Non-Ribosomal Templated, Large-Target-Spectral, Thermotolerant-Antimicrobial Peptides (by Both), and Iodinin (by EMC)

“…10 years later in another experiment [ 97 ], using another X. bovienii strain, the natural symbiont of S. jollieti , (called Xb-Sj) was a very weak antibiotic producer. It possesses a P2-like phage tail gene cluster (xbp1), that encodes genes for xenorhabdicin production (Steven A. Forst, personal communication).…”

“…In that experiment, X. szentirmaii was extremely sensitive towards the purified X. bovienii xenorhabdicin, and it did not produce effective xenorhabdicin against the X. bovienii Xb-Sj strain, at least not in poor Grace’s medium [ 97 ]. However, it was demonstrated that X. szentirmaii produced high-level antibiotic activity, which killed X. bovienii in a complete rich medium [ 97 ]. When the two species were co-cultured in either of the two media, X. szentirmaii was the winner.…”

Beyond Soil-Dwelling Actinobacteria: Fantastic Antibiotics and Where to Find Them

“…Xenocin, produced by X. nematophyla , is an RNase delivered through a type III secretion system and produced under iron deprivation conditions [ 155 , 156 ]. Xenorhabdicin, also the product of several Xenorhabdus species, is an R-type or phage tail-like bacteriocin that targets other Xenorhabdus and Photorhabdus species [ 157 , 158 , 159 ]. Together with xenocin they are proposed to inhibit competition from closely related species in the iron-deficient larval environment [ 156 ].…”