Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont

Abstract

Bacterial symbionts that undergo long-term maternal transmission experience elevated fixation of deleterious mutations, resulting in massive loss of genes and changes in gene sequences that appear to limit efficiency of gene products. Potentially, this dwindling of symbiont functionality impacts hosts that depend on these bacteria for nutrition. One evolutionary escape route is the acquisition of a novel symbiont with a robust genome and metabolic capabilities. Such an acquisition has occurred in an ancestor of Philaenus spumarius, the meadow spittlebug (Insecta: Cercopoidea), which has replaced its ancient association with the tiny genome symbiont Zinderia insecticola (Betaproteobacteria) with an association with a symbiont related to Sodalis glossinidius (Gammaproteobacteria). Spittlebugs feed exclusively on xylem sap, a diet that is low both in essential amino acids and in sugar or other substrates for energy production. The new symbiont genome has undergone proliferation of mobile elements resulting in many gene inactivations; nonetheless, it has selectively maintained genes replacing functions of its predecessor for aminoacid biosynthesis. Whereas ancient symbiont partners typically retain perfectly complementary sets of amino-acid biosynthetic pathways, the novel symbiont introduces some redundancy as it retains some pathways also present in the partner symbionts (Sulcia muelleri). Strikingly, the newly acquired Sodalis-like symbiont retains genes underlying efficient routes of energy production, including a complete TCA cycle, potentially relaxing the severe energy limitations of the xylemfeeding hosts. Although evolutionary replacements of ancient symbionts are infrequent, they potentially enable evolutionary and ecological novelty by conferring novel metabolic capabilities to host lineages.

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

“…Genome size is strongly correlated to endosymbiotic age in bacteria, especially at the onset of symbiosis, when genome reduction can be rapid (53)(54)(55)(56)(57). Most relevant to our argument here is the speed with which genome reduction has been shown to take place in Sodalisallied bacteria closely related to the γ-proteobacterial symbionts of mealybugs (34,58,59). It has been estimated that as much as 55% of an ancestral Sodalis genome was lost on the transition to endosymbiosis in a mere ∼28,000 y, barely enough time for 1% sequence divergence to accumulate between the new symbiont and a free-living relative (58).…”

“…Another solution to avoid host extinction is to replace the degenerating symbiont with a fresh one or supplement it with a new partner. Examples of symbiont replacement and supplementation are replete in insects, occurring in at least the sap-feeding Auchenorrhyncha (23,(32)(33)(34), psyllids (22,35), aphids (25,36,37), lice (38), and weevils (39,40). When viewed over evolutionary time, it becomes clear that endosymbioses can be dynamic-both genes and organisms come and go.…”

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

“…Over evolutionary time, this redundancy is eliminated, as illustrated by the perfectly complementary and nonredundant combinations of biosynthetic pathways repeatedly observed for genomes of coresident symbionts in sapfeeding insects (1,85,86). Depending on which genome initially loses specific biosynthetic capabilities, a likely outcome is that both old and new symbionts become obligate for the host, each maintaining distinct and complementary contributions.…”

“…The Sodalis-like symbiont that replaced Zinderia in spittlebugs of tribe Philaenini (Fig. 3) has a reduced genome but retains pathways complementary to those of its Sulcia partner (86). This new symbiont occupies a distinct cell type from the bacteriocytes that house Zinderia in other spittlebugs (91).…”

Evolution of host specialization in gut microbes: the bee gut as a model

“…Another open question is whether specialization destines microbes to an evolutionary dead-end due to the increased risk of extinction that result from highly restricted host ranges and the loss of functional capabilities from genome erosion. Intracellular symbionts can degenerate to the point where they are replaced, 57 but for gut microbes, the prospect of gene flow may prevent this outcome.…”