Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

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.Sodalis | organelle | horizontal gene transfer | scale insect

Quorum Sensing Attenuates Virulence in Sodalis praecaptivus

“…Close relatives of S. praecaptivus have been identified in a wide range of insect hosts (Snyder et al, 2011; Clayton et al, 2012), and genomic analyses indicate that these mutualistic symbionts have evolved repeatedly and independently from an S. praecaptivus- like antecedent, undergoing substantial genome degeneration and size reduction as a consequence of the loss of many genes that lack adaptive value following the transition to the static symbiotic lifestyle (Clayton et al, 2012; Husnik and McCutcheon, 2016). Regarding their origin, the closest relatives of S. praecaptivus have been found in certain stinkbugs and chestnut weevils, in which these bacteria have a sporadic frequency of infection among insect populations (Kaiwa et al, 2010; Toju and Fukatsu, 2011), suggesting that they are not maternally transmitted by these insects but are instead acquired horizontally from the environment by each new insect generation.…”

Can social partnerships influence the microbiome? Insights from ant farmers and their trophobiont mutualists

“…Morenella, which fulfils several essential genome functions of its own (von Dohlen et al, 2001;Husnik et al, 2013;McCutcheon & von Dohlen, 2011). Over evolutionary time, these Gammaproteobacteria have repeatedly been replaced, also with Sodalis-like bacteria (Husnik & McCutcheon, 2016). The trio of perfectly matching mealybug, Similarly, all root aphids in the system contain species-specific genotypes of Buchnera aphidicola, a well-studied, obligate primary endosymbiont of aphids, well-known for its vital metabolic functions, most importantly in the production of essential amino acids (Douglas, 1998).…”

To B or not to B: Arsenophonus as a source of B-vitamins in whiteflies

“…In the lineage Arsenophonus - Riesia , the sizes of several genomes have been reported, ranging from the 0.58 Mb of Candidatus Riesia pediculicola (Kirkness et al, 2010) and 0.84 Mb of A. lipopteni (Nováková et al, 2016) to 3.86 Mb of A. triatominarum , but with several genomes of intermediate sizes (Šochová et al, 2017). Similarly, Sodalis endosymbionts display also a large range of genome sizes, from the 0.35 Mb of Candidatus Mikella endobia (Husnik and McCutcheon, 2016) to the circa 4.5 Mb of S. glossinidius or S. pierantonius , and with several genome sizes in the range of 1-2 Mb (Santos-Garcia et al, 2017). This range has also been observed in Serratia symbiotica , with genome sizes from 0.65 to 3.86 Mb (Manzano-Marín et al, 2016).…”