Filip Husnik and John P. McCutcheon

EVOLUTION

Significance

Mealybugs are plant sap-sucking insects with a nested symbiotic arrangement, where one bacterium lives inside another bacterium, which together live inside insect cells. These two bacteria, along with genes transferred from other bacteria to the insect genome, allow the insect to survive on its nutrient-poor diet. Here, we show that the innermost bacterium in this nested symbiosis was replaced several times over evolutionary history. These results show that highly integrated and interdependent symbiotic systems can experience symbiont replacement and suggest that similar dynamics could have occurred in building the mosaic metabolic pathways seen in mitochondria and plastids.

Abstract

Stable endosymbiosis of a bacterium into a host cell promotes cellular and genomic complexity. The mealybug Planococcus citri has two bacterial endosymbionts with an unusual nested arrangement: the γ-proteobacterium Moranella endobia lives in the cytoplasm of the β-proteobacterium Tremblaya princeps. These two bacteria, along with genes horizontally transferred from other bacteria to the P. citri genome, encode gene sets that form an interdependent metabolic patchwork. Here, we test the stability of this three-way symbiosis by sequencing host and symbiont genomes for five diverse mealybug species and find marked fluidity over evolutionary time. Although Tremblaya is the result of a single infection in the ancestor of mealybugs, the γ-proteobacterial symbionts result from multiple replacements of inferred different ages from related but distinct bacterial lineages. Our data show that symbiont replacement can happen even in the most intricate symbiotic arrangements and that preexisting horizontally transferred genes can remain stable on genomes in the face of extensive symbiont turnover.

See: http://www.pnas.org/content/113/37/E5416.abstract.html?etoc

PNAS September 13 2016; vol.113; no.37:  E5416–E5424

Fig. 1.

Genome size and structure of the mealybug endosymbionts. Linear genome alignments of (Upper) seven Tremblaya genomes (blue) are contrasted with linear genome alignments of (Lower) five genomes of their respective γ-proteobacterial symbionts (red). The T. princeps genomes are perfectly collinear and similar in size, whereas the γ-proteobacterial genomes are highly rearranged and different in size. Alignments are ordered based on a schematic mealybug/Tremblaya phylogeny (original phylogenies are in Fig. S1) and accompanied by basic genome statistics (detailed genome statistics are in Table 1). Gene boxes are colored according to their category: proteins in blue, pseudogenes in gray, rRNAs in green, noncoding RNAs in yellow, and tRNAs in red.