Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

• Published in: Journal of evolutionary biology Vol. 36; no. 12; pp. 1712 - 1730
• Main Authors: Peng, Linyao, Hoban, Jessica, Joffe, Jonah, Smith, Andrew H., Carpenter, Melissa, Marcelis, Tracy, Patel, Vilas, Lynn‐Bell, Nicole, Oliver, Kerry M., Russell, Jacob A.
• Format: Journal Article
• Language: English
• Published: Switzerland Blackwell Publishing Ltd 01.12.2023
• Subjects: Acyrthosiphon pisum; Algorithms; Bacteria; Biosynthesis; Biotin; Community structure; Complementarity; evolution of cooperation; Expansion joints; Genomes; genomics; Genotyping; Hemocoel; Inactivation; Insects; Metabolism; microbes; Microbiomes; Mutualism; Peas; Questions; Rickettsiella; Serratia; Symbionts; Trends; genomics; microbes; insects; evolution of cooperation
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.14216

Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid, Acyrthosiphon pisum. Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co‐infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co‐infection trends. To test whether within‐host metabolic interactions predict common versus rare strain‐defined communities, we leveraged the high relatedness of our dominant, community‐defined symbiont strains vs. 12 pea aphid‐derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts—Serratia symbiotica and Rickettsiella viridis. Applying the expansion network algorithm, through additional use of pea aphid and obligate Buchnera symbiont genomes, Serratia and Rickettsiella emerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi‐party mutualism within their nutrient‐limited, phloem‐feeding hosts. Recent, complementary gene inactivation, within the biotin pathways of Serratia and Rickettsiella, raises further questions on the origins of mutualisms and host–symbiont interdependencies. We genotyped seven bacterial species across protein‐coding gene loci, to define common vs. rare ‘symbiont’ communities among pea aphids from the United States. Leveraging prior genome sequences from the identified strains, we tested the hypothesis that metabolic interactions among symbionts drive this ‘community structure’. We found support for this hypothesis for the symbiont pairing between the most abundant strains of Serratia symbiotica and Rickettsiella viridis. Specifically, genome‐wide analyses revealed that these two commonly partnered symbionts exhibit high, reciprocal complementarity across the metabolic pathways encoded by their genomes. Together, the two symbionts enable the pea aphid ‘holobiont’ to synthesize biotin (vitamin B7), an important vitamin found at low levels in the pea aphid diet.