Cicada endosymbionts contain tRNAs that are processed despite having genomes that lack tRNA processing activities

Leuven, James T. Van; Mao, Meng; Bennett, Gordon M.; McCutcheon, John P.

doi:10.1101/365791

Cited by 2 publications

(1 citation statement)

References 104 publications

(103 reference statements)

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“…Second, they fall on relatively short branch lengths on phylogenomic trees relative to their non-endosymbiont relatives (Figure 2), indicating that they have not yet experienced the rapid sequence evolution typical of older endosymbiotic bacteria (Moran, 1996). Third, their GC contents at 4-fold degenerate sites in coding regions remains relatively high (Supplemental File 2), whereas older endosymbionts typically show pronounced AT biases at these sites (Wernegreen, 2002;Van Leuven and McCutcheon, 2012).…”

Section: Discussionmentioning

confidence: 99%

The evolution of interdependence in a four-way mealybug symbiosis

Garber

Kupper

Laetsch

et al. 2021

Preprint

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Mealybugs are insects that maintain intracellular bacterial symbionts to supplement their nutrientpoor plant sap diets. Some mealybugs have a single betaproteobacterial endosymbiont, a Candidatus Tremblaya species (hereafter Tremblaya) that alone provides the insect with its required nutrients. Other mealybugs have two nutritional endosymbionts that together provide these nutrients, where Tremblaya has gained a gammaproteobacterial partner that resides in the cytoplasm of Tremblaya. Previous work had established that Pseudococcus longispinus mealybugs maintain not one but two species of gammaproteobacterial endosymbionts along with Tremblaya. Preliminary genomic analyses suggested that these two gammaproteobacterial endosymbionts have large genomes with features consistent with a relatively recent origin as insect endosymbionts, but the patterns of genomic complementarity between members of the symbiosis and their relative cellular locations were unknown. Here, using long-read sequencing and various types of microscopy, we show that the two gammaproteobacterial symbionts of P. longispinus are mixed together within Tremblaya cells, and that their genomes are somewhat reduced in size compared to their closest non-endosymbiotic relatives. Both gammaproteobacterial genomes contain thousands of pseudogenes, consistent with a relatively recent shift from a free-living to endosymbiotic lifestyle. Biosynthetic pathways of key metabolites are partitioned in complex interdependent patterns among the two gammaproteobacterial genomes, the Tremblaya genome, and horizontally acquired bacterial genes that are encoded on the mealybug nuclear genome. Although these two gammaproteobacterial endosymbionts have been acquired recently in evolutionary time, they have already evolved co-dependencies with each other, Tremblaya, and their insect host.SignificanceMealybugs are sap-feeding insects that house between one and three bacterial endosymbionts to supplement their nutritionally poor diets. Many mealybug-bacteria relationships were established tens or hundreds of millions of years ago, and these ancient examples show high levels host-endosymbiont genomic and metabolic integration. Here, we describe the complete genomes and cellular locations for two bacterial endosymbiont which have recently transitioned from a free-living to an intracellular state. Our work reveals the rapid emergence of metabolic interdependence between these two nascent endosymbionts, their partner bacterial co-symbiont in whose cytoplasm they reside, and their insect host cell. Our work confirms that intracellular bacteria rapidly adapt to a host-restricted lifestyle through breakage or loss of redundant genes.

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Section: Discussionmentioning

confidence: 99%

The evolution of interdependence in a four-way mealybug symbiosis

Garber

Kupper

Laetsch

et al. 2021

Preprint

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Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host

Mao

Yang

Bennett

2018

Proc. Natl. Acad. Sci. U.S.A.

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SignificanceNutritional symbionts in sap-feeding insects are characterized by highly degenerate genomes. It is poorly understood how hosts evolve to maintain these symbionts, particularly when hosts rely on more than one symbiont that requires distinct support for basic cell functions. We show that the aster leafhopper (Macrosteles quadrilineatus), which depends on two symbionts with tiny genomes (Sulcia and Nasuia), has differentially reprogramed gene-expression patterns in symbiont-associated cells. The host has acquired novel genetic traits and likely recruited preexisting mitochondrial support mechanisms to meet the specific needs of each symbiont. Broad comparisons across anciently diverged sap-feeding hosts reveal that the evolution of symbiont support mechanisms is largely unique to each host lineage. Important parallels are further observed with organelle evolution.

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Cicada endosymbionts contain tRNAs that are processed despite having genomes that lack tRNA processing activities

Cited by 2 publications

References 104 publications

The evolution of interdependence in a four-way mealybug symbiosis

The evolution of interdependence in a four-way mealybug symbiosis

Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host

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