Parallel evolution of fish bi-modal breathing and expansion of olfactory receptor (OR) genes: toward a universal ORs nomenclature

Elsevier

Available online 17 March 2023

Journal of Genetics and GenomicsAuthor links open overlay panel, , , , Abstract

Olfactory receptors (ORs) play a key role in the prime sensorial perception, being highly relevant for intra/interspecific interactions. ORs are a subgroup of G-protein coupled receptors that exhibit highly complex subgenomes in vertebrates. However, OR repertoires remain poorly studied in fish lineages, precluding finely retracing their origin, evolution and diversification, especially in the most basal groups. Here, we conducted an exhaustive gene screening upon 43 high-quality fish genomes exhibiting varied gene repertoires (2 to 583 genes). While the early vertebrates performed gas exchange through gills, we hypothesize that the emergence of new breathing structures (swim bladder and paired lungs) in early osteichthyans may be associated to expansions in the ORs gene families sensitive to airborne molecules. Additionally, we verified that the OR repertoire of moderns actinopterygians has not increased as expected following a whole genome duplication, likely due to regulatory mechanisms compensating the gene load excess. Finally, we identified 25 distinct OR families, allowing us to propose an updated universal nomenclature for the fish ORs.

Section snippetsCRediT author statement

Liliana Silva: Conceptualization, Methodology, Writing – Original draft; Tito Mendes: Conceptualization, Methodology, Writing – Original draft; Luana Ramos: Writing – Review & Editing; Guojie Zhang: Writing – Review & Editing; Agostinho Antunes: Writing – Review & Editing; Funding acquisition; Supervision.

OR family nomenclature, distribution and expansion/contraction patterns

We retrieved 5143 intact OR sequences, 277 putative OR pseudogenes, and 79 truncated sequences that resulted from the abrupt end of the contig/scaffold (Supplementary File S1). Intact OR sequences were used for a general phylogenetic reconstruction and the proposal of a new, in-depth, and integrative OR classification system (Fig. 1A). For the naming of each OR family identified in the present study, we maintained, whenever it was possible, the classification proposed by Alioto and Ngai (2005)

A new and integrative fish OR classification system – towards a universal OR nomenclature

Our study considers a high-scale search of the entire OR repertoire throughout 43 representative genomes of jawless, cartilaginous, and bony fishes. Such broader sampling strategy enlightened our understanding of the fish ORs evolution and enabled us to propose a more complete, detailed and standardized classification system (Alioto and Ngai, 2005; Niimura, 2009; Olender et al., 2020), while still accommodating the previous nomenclatures whenever possible. Those were developed based on reduced

Data collection

In order to explore the diversity of ORs throughout the major fish lineages, we performed a representative genome sampling from jawless (Cyclostomata, N = 5), cartilaginous (Chondrichthyes, N = 10) and bony (Sarcopterygii: N = 3; and Actinopterygii: N = 25) fishes. Despite the high number of available actinopterygian genomes, we selected the 25 that best represented the most basal subclasses of ray-finned fishes and had available high-quality genome assemblies’ level. All genomes were collected

OR synteny

The genomic location of each extracted OR sequence was compiled in the Supplementary File S1. ORs were considered as belonging to same gene cluster when the distance between the two sequences was less than one megabase (Wang et al., 2021) (Supplementary File S2). The comparative analysis of homologous syntenic blocks that contained OR gene clusters was performed between the cyclostoms L. reissneri and P. marinus, and between the actinopterygian species C. auratus and D. rerio, all presenting

Declaration of Competing Interest

The authors declare no competing interests.

Acknowledgments

We would like to thank all the constructive comments and suggestions provided by the three anonymous reviewers, which greatly improved the quality of this work. We thank all the useful and constructive comments provided by colleagues of the Evolutionary Genomics and Bioinformatics Group of CIIMAR (University of Porto) on a previous version of this manuscript. This work was supported by a PhD grant from “Fundação para a Ciência e a Tecnologia” (FCT) (L.S.: SFRH/BD/134565/2017;

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© 2023 Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Limited and Science Press.

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