Biology subjects

Leys, S. P.

Publications and source records attributed to Leys, S. P..

4 recordsLinked to original sources

bioRxiv2026

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

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.

evolutionary biology↗

bioRxiv2025

Genomic connectivity and adaptation signals of the freshwater sponge Ephydatia muelleri across its distribution

1.Freshwater sponges fulfill critical ecological functions, including maintaining water quality, regulating nutrient dynamics, offering habitats for diverse taxa, and serving as a vital food source for various species. However, their patterns of dispersal and genetic connectivity remain inadequately understood, posing significant challenges to effective conservation assessments. We examined genetic connectivity and genetic adaptation to local environmental conditions in Ephydatia muelleri across its geographic range using ddRADseq-derived SNPs from 106 individuals collected from 11 localities spanning North America, Europe, and Asia. Analysis of 3,182 neutral SNPs revealed low connectivity and strong genetic structure among regions within two main genetic clusters of North America and Eurasia, while 115 SNPs identified to be under selection showed considerable evidence for differentiated, polygenic adaptation to light and temperature conditions across sampled locations, as well as selection on gene regulatory processes. These findings align with the "monopolization hypothesis", suggesting that historical climatic and geological conditions of the Last Glacial Maximum, including habitat expansion, contraction, and natural barriers, have contributed more to the current genetic structure of E. muelleri populations than contemporary gene flow, which is restricted by monopolistic habitat colonization by this species. Our results provide novel support for ecological theory on dispersal in aquatic invertebrates, as well as insights into the plasticity of E. muelleri in the face of varying environmental conditions that are fundamentally important for freshwater ecosystem conservation.

evolutionary biology↗

bioRxiv2024

ATP and glutamate coordinate contractions in the freshwater sponge Ephydatia muelleri

Sponges (phylum Porifera) are an early diverging animal lineage that lacks both conventional nervous and muscular systems, and yet they are able to produce coordinated whole-body contractions in response to disturbances. Little is known about the underlying signaling mechanisms in coordinating such responses. Previous studies demonstrated that sponges respond specifically to neuroactive chemicals such as L-glutamate and {gamma}-amino-butyric acid (GABA), which trigger and prevent contractions respectively. Genes for purinergic P2X-like receptors are present in several sponge genomes, leading us to ask whether ATP works with glutamate to coordinate contractions in sponges as it does in other animal nervous systems. Using pharmacological approaches on the freshwater sponge Ephydatia muelleri, we show that ATP is involved in coordinating contractions. Bath applications of ATP cause a rapid, sustained expansion of the excurrent canals in a dose-dependent manner. Complete contractions occur when ATP is added in the presence of apyrase, an enzyme that hydrolyzes ATP. Applying ADP, the first metabolic product of ATP hydrolysis, triggers complete contractions, whereas AMP, the subsequent metabolite, does not trigger a response. Blocking ATP from binding and activating P2X receptors with pyridoxalphosphate-6-azophenyl-2,4-disulfonic acid (PPADS) prevents both glutamate- and ATP-triggered contractions, suggesting that ATP works downstream of glutamate. Bioinformatic analysis revealed two P2X receptor sequences, one which groups with other vertebrate P2X receptors. Altogether, our results confirm that purinergic signaling by ATP is involved in coordinating contractions in the freshwater sponge suggesting a role of ATP-mediated signaling that predates the evolution of the nervous system and multicellularity in animals. Summary statementNerveless sponges coordinate a sneeze-like reflex using glutamate and ATP signaling to expel water from the body.

physiology↗

bioRxiv2022

The compact genome of the sponge Oopsacas minuta (Hexactinellida) is lacking key metazoan core genes

BackgroundBilaterian animals today represent 99% of animal biodiversity. Elucidating how bilaterian hallmarks emerged is a central question of animal evo-devo and evolutionary genomics. Studies of non-bilaterian genomes have suggested that the ancestral animal already possessed a diversified developmental toolkit, including some pathways required for bilaterian body plans. Comparing genomes within the early branching metazoan Porifera phylum is key to identify which changes and innovations contributed to the successful transition towards bilaterians. ResultsHere, we report the first whole genome comprehensive analysis of a glass sponge, Oopsacas minuta, a member of the Hexactinellida. Studying this class of sponge is evolutionary relevant because it differs from the three other Porifera classes in terms of development, tissue organization, ecology and physiology. Although O. minuta does not exhibit drastic body simplifications, its genome is among the smallest animal genomes sequenced so far, surprisingly lacking several metazoan core genes (including Wnt and several key transcription factors). Our study also provided the complete genome of the symbiotic organism dominating the associated microbial community: a new Thaumarchaeota species. ConclusionsThe genome of the glass sponge O. minuta differs from all other available sponge genomes by its compactness and smaller number of predicted proteins. The unexpected losses of numerous genes considered as ancestral and pivotal for metazoan morphogenetic processes most likely reflect the peculiar syncytial organization in this group. Our work further documents the importance of convergence during animal evolution, with multiple emergences of sponge skeleton, electrical signaling and multiciliated cells.

evolutionary biology↗