Lateral gene transfer introduced the microbial anaerobiosis-related gene rquA into early animals

Abstract

Lateral gene transfer (LGT) enables rapid metabolic innovation in microbes, but its evolutionary importance in animals remains debated. Among metabolic traits with major ecological consequences, adaptations to low-oxygen conditions often involve modifications of mitochondrial electron transport and the quinones that mediate electron flow. Rhodoquinone-based anaerobic metabolism occurs in several eukaryotic lineages, yet the evolutionary routes by which animals acquired this capability are poorly understood. Here we show that freshwater sponges possess a rhodoquinone biosynthesis gene, rquA, previously restricted to microbial lineages, which was acquired by lateral gene transfer and functionally integrated into sponge metabolism. Heterologous expression of rquA from the model freshwater sponge Ephydatia muelleri enables rhodoquinone production in yeast, consistent with functional conservation. In E. muelleri, the rquA gene is upregulated under hypoxia and rhodoquinone is detectable across all lifestages, however, it is most abundant in early development in the pluiripotent gemmules. Using comparative genomics, we find that the presence of rquA in freshwater sponges correlates with loss of key genes of the ubiquinone biosynthesis pathway, suggesting these animals cannot synthesize ubiquinone de novo and we show that E. muelleri can convert exogenous ubiquinone to rhodoquinone. Rhodoquinone levels were significantly higher in rquA-encoding freshwater sponges compared to marine sponges that were sampled from natural environments. This study reveals that an early animal lineage acquired a microbial metabolism-related gene via lateral gene transfer during or before the transition to freshwater environments, enabling rhodoquinone utilization and potentially enhancing tolerance to oxygen fluctuations. Thereby, demonstrating how LGT shapes energy metabolism even in multicellular organisms.