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 amino-acid 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 xylem-feeding hosts. Although evolutionary replacements of ancient symbionts are infrequent, they potentially enable evolutionary and ecological novelty by conferring novel metabolic capabilities to host lineages.

Figure 1

Comparison of genomes of the two P. spumarius symbionts (upper half in a and b) with previously sequenced genomes of related bacterial species (lower half in a and b). (a) Genome of Sulcia muelleri-PSPU compared with that of S. muelleri-CARI, showing arrangement and orientation of open reading frames, GC content, and GC skew. The two Sulcia genomes are completely syntenic except for a few genes present in one and not the other. (b) Genome of SLs-PSPU compared with that of Sodalis glossinidius, including its three plasmids. The innermost graph of SLs-PSPU shows concatenated scaffolds arranged according to position in the S. glossinidius genome; scaffolds are distinguished by colors and homology to sequences in the S. glossinidius is indicated by lines of the same color.

Figure 2

Sequences of SLs-PSPU that are derived from IS elements and phages, showing their relative locations in the S. glossinidius genome. A concatenated representation of scaffolds derived from SLs-PSPU is shown at the top with each scaffold in a different color. IS elements and phages identified within the S. glossinidius genome and identified by Belda et al. (2010) are shown with gray bands on the bar representing the S. glossinidius genome. Among them, those showing significant similarities to the SLs scaffolds are labeled with their name and colored as indicated at the bottom of the figure. Names of IS elements and phages proposed by Belda et al. (2010) were adopted. In the legends, the family name of the IS elements are in parentheses. Portions of ISsgl8 (IS1 family) are present as a single copy in the S. glossinidius genome but found on 235 scaffolds in the SLs-PSPU genome.

Figure 3

Reconstruction of symbiont-based metabolism in P. spumarius showing reactions for which SLs and Sulcia possess intact genes. (a) Pathways for amino-acid biosynthesis and energy production. (b) Hypothesized movement of molecules between compartments for SLs and Sulcia, showing route for production of glutamic acid used for producing TCA cycle intermediates.

Figure 4

Hypothesized evolutionary sequence leading to current symbiotic associations of Philaenus spumarius, showing events discussed in text. Timescale is approximate, and dates are based on Cryan and Svenson (2010). Representative insect species for which symbiont genomes were sequenced in previous studies are Macrosteles quadrilineatus (Bennett and Moran, 2013), Homalodisca vitripennis (McCutcheon and Moran, 2007) and Clastoptera arizonana (McCutcheon and Moran, 2010).