Defensive Bacteriome Symbiont with a Drastically Reduced Genome

Abstract

Diverse insect species harbor symbiotic bacteria, which play important roles such as provisioning nutrients and providing defense against natural enemies [1-6]. Whereas nutritional symbioses are often indispensable for both partners, defensive symbioses tend to be of a facultative nature [1-12]. The Asian citrus psyllid Diaphorina citri is a notorious agricultural pest that transmits Liberibacter spp. (Alphaproteobacteria), causing the devastating citrus greening disease or Huanglongbing [13, 14]. In a symbiotic organ called the bacteriome, D. citri harbors two distinct intracellular symbionts: a putative nutrition provider, Carsonella_DC (Gammaproteobacteria), and an unnamed betaproteobacterium with unknown function [15], for which we propose the name "Candidatus Profftella armatura." Here we report that Profftella is a defensive symbiont presumably of an obligate nature with an extremely streamlined genome. The genomes of Profftella and Carsonella_DC were drastically reduced to 464,857 bp and 174,014 bp, respectively, suggesting their ancient and mutually indispensible association with the host. Strikingly, 15% of the small Profftella genome encoded horizontally acquired genes for synthesizing a novel polyketide toxin. The toxin was extracted, pharmacologically and structurally characterized, and designated diaphorin. The presence of Profftella and its diaphorin-biosynthetic genes was perfectly conserved in the world's D. citri populations.

Infection Density Dynamics of the Citrus Greening Bacterium “Candidatus Liberibacter asiaticus” in Field Populations of the Psyllid Diaphorina citri and Its Relevance to the Efficiency of Pathogen Transmission to Citrus Plants

“…For example, considering that D. citri harbors two bacteriome-associated obligate endosymbionts (Carsonella and Profftella) and other facultative endosymbionts (Wolbachia and Arsenophonus, etc.) (37)(38)(39)(40)(41), it is conceivable, although speculative, that these coexisting endosymbionts may also affect "Ca. Liberibacter asiaticus" infection densities in D. citri populations.…”

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

“…In some psyllids, Carsonella shows metabolic interdependence with coresident symbionts (57). In each case, the newer obligate symbiont is subject to the same genome decay process as the older symbiont (87,90,94,100).…”

Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula”

“…Portions of the bry pathway for the bryostatins were recovered previously using clone library methods (6), but the complete genome sequence, including missing pieces of the bry pathway, has remained elusive due to recalcitrance of the symbiont to culture. A number of factors are thought to contribute to this recalcitrance, including the possibility of substantial genome reduction (7), which has been reported in other invertebrate symbioses (14)(15)(16). Indeed, the divergence of symbionts in genetically isolated hosts (17), as well as restriction to B. neritina and allied species, the vertical mode of symbiont transmission, and the ongoing inability to isolate and culture "Ca.…”

“…Endobugula sertula" in order to determine whether the symbiosis has evolved to a state of codependency, evidenced by bacterial genome degradation, as in some other defensive symbioses (14)(15)(16). Shotgun DNA and RNA sequencing revealed a genome with few signs of reduction, largely intact mainstream metabolic pathways, and a putative mechanism of vertical transmission of "Ca.…”