# Horizontally Transferred Carotenoid Genes Associated with Light-Driven ATP Synthesis to Promote Cold Adaptation in Pea Aphid, Acyrthosiphon pisum

## TL;DR

Pea aphids use carotenoid pigments from fungi to capture light energy and boost energy production in cold conditions, improving their survival and reproduction.

## Contribution

Discovery of a novel light-driven energy mechanism in aphids via horizontally transferred fungal genes under cold stress.

## Key findings

- High light intensity at cold temperatures increases ATP content by 240% in pea aphids.
- Carotenoid pigments enhance aphid reproduction and development under cold stress.
- The energy mechanism is inactive at warmer temperatures, indicating a temperature-gated system.

## Abstract

The pea aphid, Acyrthosiphon pisum, is a major agricultural pest. It uniquely possesses fungal-derived genes that allow it to produce carotenoid pigments typically found in plants. Our study reveals a previously unknown role for these pigments beyond coloration. Under cold stress (12 °C), high light intensity triggers carotenoids to act like micro solar panels, capturing light to fuel ATP production. This leads to a striking 240% boost in energy, enhancing aphid development and reproduction under cold conditions. In contrast, the system remains inactive at warmer temperatures (22 °C). These findings demonstrate how a single horizontal gene transfer event can provide an organism with a novel energy-capturing ability, markedly increasing its adaptability in variable environments.

The pea aphid, Acyrthosiphon pisum, possesses horizontally acquired fungal carotenoid biosynthesis genes, enabling de novo production of carotenoids. Although carotenoids are known to contribute to photo-protection and coloration, their potential role in energy metabolism and population fitness under thermal stress is still unclear. This study investigated the interactive effects of temperature and light intensity on energy homeostasis and life-history traits in A. pisum. Using controlled environmental regimes, we demonstrate that light intensity significantly influenced the ATP content, development, and reproductive output of A. pisum at 12 °C, but not at 22 °C. Under cold stress (12 °C), high light intensity (5000 lux) increased ATP content by 240%, shortened the pre-reproductive period by 46%, extended reproductive duration by 62%, and enhanced the net reproductive rate (R0) and intrinsic rate of increase (rₘ) compared to low light intensity (200 lux). These effects were abolished at the optimal temperature (22 °C), indicating a temperature-gated, light-dependent mechanism. Demographic analyses revealed that carotenoid-associated solar energy harvesting significantly improves fitness under cold conditions, likely compensating for metabolic depression. Our findings reveal a novel ecological adaptation in aphids, where horizontally transferred genes may enable light-driven energy supplementation during thermal stress. This study provides new insights into the physiological mechanisms underlying insect resilience to climate variability and highlights the importance of light as a key environmental factor in shaping life-history strategies in temperate agroecosystems.