Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

Abstract

Many insects depend on obligate mutualistic bacteria to provide essential nutrients lacking from their diet. Most aphids, whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera aphidicola to supply essential amino acids and B vitamins. However, in some aphid species, provision of these nutrients is partitioned between Buchnera and a younger bacterial partner, whose identity varies across aphid lineages. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. It is also unclear whether the novel symbionts merely compensate for losses in Buchnera or carry new nutritional functions. Using whole-genome endosymbiont sequences of nine Cinara aphids that harbour an Erwinia-related symbiont to complement Buchnera, we show that the Erwinia association arose from a single event of symbiont lifestyle shift, from a free-living to an obligate intracellular one. This event resulted in drastic genome reduction, long-term genome stasis, and co-divergence with aphids. Fluorescence in situ hybridisation reveals that Erwinia inhabits its own bacteriocytes near Buchnera's. Altogether these results depict a scenario for the establishment of Erwinia as an obligate symbiont that mirrors Buchnera's. Additionally, we found that the Erwinia vitamin-biosynthetic genes not only compensate for Buchnera's deficiencies, but also provide a new nutritional function; whose genes have been horizontally acquired from a Sodalis-related bacterium. A subset of these genes have been subsequently transferred to a new Hamiltonella co-obligate symbiont in one specific Cinara lineage. These results show that the establishment and dynamics of multi-partner endosymbioses can be mediated by lateral gene transfers between co-ocurring symbionts.

Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

“…Because of its strict vertical transmission, Buchnera has undergone long-term coevolution with its aphid hosts [5]. However, due to the metabolic losses caused by rapid genome deterioration in Buchnera [6], some aphid species of the subfamilies Lachninae, Chaitophorinae, and Aphidinae have established co-obligate associations with other symbiotic partners [7,8].…”

The Bacterial Flora Associated with the Polyphagous Aphid Aphis gossypii Glover (Hemiptera: Aphididae) Is Strongly Affected by Host Plants

“…More details are reviewed in Oliver et al [44], Zytynska and Weisser [45], and Guo et al [46]. In addition, several facultative symbionts seem to have established coobligate associations along with Buchnera in certain aphid species, such as Serratia symbiotica, Erwinia haradaeae, Fukatsuia symbiotica, Hamiltonella defensa, and Sodalis in some Lachninae species [21,[47][48][49][50][51] and Wolbachia in Pentalonia nigronervosa [52,53].…”

Dynamics of Insect–Microbiome Interaction Influence Host and Microbial Symbiont

“…However, it has been now shown that these ancient symbionts establish a di-symbiotic relationship with newly acquired bacterial species. Manzano-Marín et al (2020) have reported that Erwinia, (which is a newly acquired symbiont of aphids) complements Buchnera (an ancient symbiont) by serial horizontal transfer of several vitamin biosynthesis genes and thus, compensating for the massive gene loss undergone by Buchnera during the long period of its association with its insect host. Similarly, a horizontal gene transfer event was observed between Cardinium and its donor organisms, Wolbachia and Rickettsia, which counterbalance the significant gene loss undergone by Cardinium to adapt to the gut environment of its host (Zeng et al, 2018).…”