Biology subjects

Martin-Zamora, F. M.

Publications and source records attributed to Martin-Zamora, F. M..

3 recordsLinked to original sources

bioRxiv2022

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones. TeaserGenome reduction and adaptations for collagen digestion underpin the symbiosis of Osedax worms to exploit decaying bones.

genomics↗

bioRxiv2022

The Fox gene repertoire in the annelid Owenia fusiformis reveals multiple expansions of the foxQ2 class in Spiralia

Fox genes are a large and conserved family of transcription factors involved in many key biological processes, including embryogenesis and body patterning. Although the role of Fox genes has been studied in an array of model systems, comprehensive comparative studies in Spiralia--a large clade of invertebrate animals including molluscs and annelids--are scarce but much needed to better understand the evolutionary history of this gene family. Here, we reconstruct and functionally characterise the Fox gene complement in the annelid Owenia fusiformis, a slow evolving species and member of the sister group to all remaining annelids. The genome of O. fusiformis contains at least a single ortholog of each of the 23 Fox gene classes that are ancestral to Bilateria, except for foxE and foxI. Temporal and spatial expression dynamics reveal a conserved role of Fox genes in gut formation (foxA), mesoderm patterning (foxF, foxL1, foxC, foxH) and cilia formation (foxJ1) in Annelida and Spiralia. Moreover, we uncover an ancestral expansion of foxQ2 genes in Spiralia, represented by 11 paralogs in O. fusiformis. Notably, although all foxQ2 copies have apical expression in O. fusiformis, they show variable spatial domains and staggered temporal activation, which suggest cooperation and sub-functionalisation among foxQ2 genes for the development of apical fates in this annelid. Altogether, our study informs the evolution and developmental roles of Fox genes in Annelida and Spiralia generally, providing the basis to explore how regulatory changes in Fox gene expression might have contributed to developmental and morphological diversification in Spiralia. Significance statementThe role of Fox genes, a group of DNA-binding proteins required for the formation of many animal organs, is poorly understood in invertebrate groups such as molluscs and annelids. Here, by studying the genome and embryogenesis of the annelid Owenia fusiformis, we demonstrate that Fox genes are involved in the development of the gut, muscles, cilia, and nervous system. Importantly, we find that a group of Fox genes (referred to as foxQ2) expressed in the anterior end of most animals has more copies in annelids and molluscs than in other invertebrate groups like insects and sea stars. Together, our findings clarify the evolution of Fox genes and their contribution to the diversity of forms and organs found in marine invertebrates.

evolutionary biology↗

bioRxiv2022

Annelid functional genomics reveal the origins of bilaterian life cycles

Indirect development with an intermediate larva exists in all major animal lineages1, making larvae central to most scenarios of animal evolution2-12. Yet how larvae evolved remains disputed. Here we show that temporal shifts (i.e., heterochronies) in trunk formation underpin the diversification of larvae and bilaterian life cycles. Combining chromosome-scale genome sequencing in the slow-evolving annelid Owenia fusiformis13 with transcriptomic and epigenomic profiling during the life cycles of this and two other annelids, we found that trunk development is deferred to pre-metamorphic stages in the feeding larva of O. fusiformis, but starts after gastrulation in the non-feeding larva with gradual metamorphosis of Capitella teleta and the direct developing embryo of Dimorphilus gyrociliatus. Accordingly, the embryos of O. fusiformis develop first into an enlarged anterior domain that forms larval tissues and the adult head. Notably, this also occurs in the so-called "head larvae" of other bilaterians14,15, with whom O. fusiformis larva shows extensive transcriptomic similarities. Together, our findings suggest that the temporal decoupling of head and trunk formation, as maximally observed in "head larvae", allowed larval evolution in Bilateria, thus diverging from prevailing scenarios that propose either co-option10,11 or innovation12 of gene regulatory programmes to explain larva and adult origins.

genomics↗