Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiontBuchnerain an aphid

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.

Population dynamics of defensive symbionts in aphids

“…The experiment was carried out for a minimum of 18 months after the most recent artificial infection (UT1/5A). Thus, previous findings of reduced fitness of A. pisum within the first eight months following establishment of an artificial infection (Koga et al 2003) are unlikely to be a concern here. We established six population cages, each with an equal number and proportion of A. pisum representing three infection states: uninfected with SS (line 5A), infected with S. symbiotica (2BB/5A) and infected with Hamiltonella (UT1/5A).…”

Bacterial symbionts in insects or the story of communities affecting communities

“…In such circumstances, symbionts monopolizing resources should be selected for at the within-host level, if this increases the efficiency of their own vertical transmission. Examples of such competitive interactions have been illustrated between secondary symbionts [6,102], but also in situations of co-infections between primary and secondary symbionts [103,104]. If symbionts evolve higher competitive ability, this may further limit the maintenance of multiple infections.…”

Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi

“…Importantly, the fluorescent signal of the probes BLOsADf2 (Desirò et al, 2013) and CaGgADf1 was always co-localized with the fluorescence given by the universal bacterial probe EUB338 (Amann et al, 1990) (Figures 5b-e). No fluorescent signal was detected with the negative control probe ApisP2a (Koga et al, 2003) (Figure 5i). Pre-treatment with RNase, as well as control hybridization with nonsense probes, did not provide any FISH signal.…”

“…The Mre-specific probe BLOsADf2 (Desirò et al, 2013), together with a newly designed CaGg-specific 16S rRNA probe (CaGgADf1 5 0 -CTATCCCCCTCTACAGGAYAC-3 0 ), were used to label the endobacteria. In addition, the eubacterial probe EUB338 (Amann et al, 1990) and the Buchnera-specific probe ApisP2a (Koga et al, 2003) were used. Spores were observed using a Leica TCS-SP2 confocal microscope (Leica Microsystems).…”