Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont<i>Buchnera</i>in an aphid

TLDR

Aphids depend on the essential endosymbiont Buchnera aphidicola, which supplies nutrients and supports host growth, but loss of Buchnera causes growth retardation and sterility due to its highly integrated mutualism. We found that the facultative symbiont pea aphid secondary symbiont (PASS) can replace Buchnera, allowing Buchnera‑free aphids to survive and reproduce, yet it suppresses Buchnera in normal hosts, revealing complex symbiont interactions and a potential evolutionary pathway toward new obligate endosymbiosis.

Abstract

Almost all aphids harbour an endosymbiotic bacterium, Buchnera aphidicola, in bacteriocytes. Buchnera synthesizes essential nutrients and supports growth and reproduction of the host. Over the long history of endosymbiosis, many essential genes have been lost from the Buchnera genome, resulting in drastic genome reduction and the inability to live outside the host cells. In turn, when deprived of Buchnera, the host aphid suffers retarded growth and sterility. Buchnera and the host aphid are often referred to as highly integrated almost inseparable mutualistic partners. However, we discovered that, even after complete elimination of Buchnera, infection with a facultative endosymbiotic gamma-proteobacterium called pea aphid secondary symbiont (PASS) enabled survival and reproduction of the pea aphid. In the Buchnera-free aphid, PASS infected the cytoplasms of bacteriocytes that normally harbour Buchnera, establishing a novel endosymbiotic system. These results indicate that PASS can compensate for the essential role of Buchnera by physiologically and cytologically taking over the symbiotic niche. By contrast, PASS negatively affected the growth and reproduction of normal host aphids by suppressing the essential symbiont Buchnera. These findings illuminate complex symbiont-symbiont and host-symbiont interactions in an endosymbiotic system, and suggest a possible evolutionary route to novel obligate endosymbiosis by way of facultative endosymbiotic associations.