The boom and bust of the aphid’s essential amino acid metabolism across nymphal development

Abstract

Within long term symbioses animals integrate their physiology and development with their symbiont. In a model nutritional mutualism, aphids harbor the endosymbiont, Buchnera, within specialized bacteriocyte cells. Buchnera synthesizes essential amino acids (EAA) and vitamins for their host, which are lacking from the aphid’s plant sap diet. It is unclear if the aphid host differentially expresses aphid EAA metabolism pathways and genes that collaborate with Buchnera for the production of EAA and vitamins throughout nymphal development when feeding on plants. It is also unclear if aphid bacteriocytes are differentially methylated throughout aphid development as DNA methylation may play a role in gene regulation. By analyzing aphid gene expression, we determined that the bacteriocyte is metabolically more active in metabolizing Buchnera’s EAAs and vitamins early in nymphal development compared to intermediate or later immature and adult lifestages. The largest changes in aphid bacteriocyte gene expression, especially for aphid genes that collaborate with Buchnera, occurred during the 3rd to 4th instar transition. During this transition there is a huge shift in the bacteriocyte from a high energy ‘nutrient-consuming state’ to a ‘recovery and growth state’ where patterning and signaling genes and pathways are upregulated and differentially methylated, and de novo methylation is reduced as evidenced by homogenous DNA methylation profiles after the 2nd instar. Moreover, bacteriocyte number increased and Buchnera’s titer decreased throughout aphid nymphal development. These data suggest in combination that bacteriocytes of older nymphal and adult lifestages depend less on the nutritional symbiosis compared to early nymphal lifestages.

Effects of Host Plant and Insect Generation on Shaping of the Gut Microbiota in the Rice Leaffolder, Cnaphalocrocis medinalis

“…Enterobacteriaceae is one of the important dominant taxa in the gut microbiota of many insects ( Wang et al, 2014 ; Yun et al, 2018 ; Raza et al, 2020 ). Enterobacteriaceae are involved in insect metabolism ( Pers and Hansen, 2021 ; Zhou et al, 2021 ), insect resistance or susceptibility to parasites, and pathogens and insecticides ( Oliver et al, 2003 ; Álvarez-Lagazzi et al, 2021 ; Polenogova et al, 2021 ) and play an important role in the host adaptability and reproduction of insects ( Shi et al, 2012 ; Wang et al, 2020b ). Pectobacterium , a clade of Enterobacteriaceae , is known as a function of nitrogen fixation ( Behar et al, 2005 , 2008 ).…”

Potato leafroll virus reduces Buchnera aphidocola titer and alters vector transcriptome responses

“…A decrease in Buchnera titer has previously been associated with different aphid clones 83 , plant diets 13 , increasing aphid nymphal age 82 , 84 , and heat shock 81 , 84 , 86 . Most obligate pathogens and symbionts, including Buchnera, overexpress the protein GroEL during non-heat shock conditions to rescue misfolded proteins 87 .…”

Ploidy dynamics in aphid host cells harboring bacterial symbionts

“…Our findings in this study raise the possibility that bacteriocyte polyploidy can enhance nutritional symbiosis between aphids and B. aphidicola , wherein both supply each other with nutrients that they cannot synthesize on their own [10, 19, 20] . Specifically, we predict that genes involved in amino acid metabolism, related to transport, and for symbiont regulation (e.g., lysozymes or cysteine-rich secreted proteins targeting bacteria), which have been reported to be highly expressed in the aphid bacteriomes [24, 25, 38, 40] , may be upregulated in a ploidy-dependent manner [6, 7, 47] . On the other hand, it is commonly known that cell volumes change depending on ploidy levels [6, 48] .…”

“…Pea-aphid, Acyrthosiphon pisum (Harris), is one of the best-studied aphid species in terms of life history (Figure 2, [29,30] ), polymorphism (Figure S1, [30][31][32] ), embryonic development [33][34][35] , nutritional symbiosis [23][24][25][36][37][38] , and genomics [39][40][41] . Detailed descriptions have focused on bacteriocyte development during aphid embryogenesis [21,22] , and it has been revealed that the number and volume of pea-aphid bacteriocytes increase during post-embryonic development ( [38,42] but see [43,44] ). These observations imply that aphid bacteriocytes are already polyploid at the end of embryogenesis and become hyper polyploid during post-embryonic development.…”