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Introduction: Mudskippers are a large group of amphibious fishes that have developed many morphological and physiological capacities to live on land. Genomics comparisons of chromosome-level genome assemblies of three representative mudskippers, Boleophthalmus pectinirostris (BP), Periophthalmus magnuspinnatus (PM) and P. modestus (PMO), may be able to provide novel insights into the water-to-land evolution and adaptation. Methods: Two chromosome-level genome assemblies for BP and PM were respectively sequenced by an integration of PacBio, Nanopore and Hi-C sequencing. A series of standard assembly and annotation pipelines were subsequently performed for both mudskippers. We also re-annotated the PMO genome, downloaded from NCBI, to obtain a redundancy-reduced annotation. Three-way comparative analyses of the three mudskipper genomes in a large scale were carried out to discover detailed genomic differences, such as different gene sizes, and potential chromosomal fission and fusion events. Comparisons of several representative gene families among the three amphibious mudskippers and some other teleosts were also performed to find some molecular clues for terrestrial adaptation. Results: We obtained two high-quality haplotype genome assemblies with 23 and 25 chromosomes for BP and PM respectively. We also found two specific chromosome fission events in PM. Ancestor chromosome analysis has discovered a common fusion event in mudskipper ancestor. This fusion was then retained in all the three mudskipper species. A loss of some SCPP (secretory calcium-binding phosphoprotein) genes were identified in the three mudskipper genomes, which could lead to reduction of scales for a part-time terrestrial residence. The loss of aanat1a gene, encoding an important enzyme (arylalkylamine N-acetyltransferase 1a, AANAT1a) for dopamine metabolism and melatonin biosynthesis, was confirmed in PM but not in PMO (as previously reported existence in BP), suggesting a better air vision of PM than both PMO and BP. Such a tiny variation within the genus Periophthalmus exemplifies to prove a step-by-step evolution for the mudskippers’ water-to-land adaptation. Conclusion: These high-quality mudskipper genome assemblies will become valuable genetic resources for in-depth discovery of genomic evolution for the terrestrial adaptation of amphibious fishes.

Aquaculture, as a rapidly growing industry, plays a significant role in global food production and economic development. However, various infectious diseases, particularly those caused by the gram-negative bacterium Aeromonas hydrophila, pose a critical threat to the sustainability and productivity of world-wide aquaculture operations. Investigating the molecular mechanisms of A. hydrophila infection can help to identify key targets for therapeutic interventions and vaccines, thereby reducing economic losses associated with disease outbreaks. Our present study focuses on wide-bodied sand loach (WBSL, Sinibotia reevesae), a captive-bred commercial fish, to explore detailed molecular effects of exogenous A. hydrophila infection. Firstly, a high-quality chromosome-level haplotype genome with a total length of 774 Mb and 49 chromosomes was assembled, providing valuable insights into its genetic components. Secondly, we isolated and characterized a newfound A. hydrophila F4S strain, examined pathological symptoms of WBSL after infection, and then investigated dynamic gene expressions. Our results revealed that the bacterial infection decreased metabolic activity, causing disruptions in cardiac function, cellular homeostasis, tissue damages, and impaired energy utilization. The immune system responds multifaceted, potentially impacting overall health and survival. In summary, our findings contribute to the understanding of the complicated interactions between WBSL and exogenous A. hydrophila, especially shed lights on the genetic complexity, immune responses, and potential impacts on fish health and survival. Furthermore, this study provides new insights into the mechanisms underlying A. hydrophila infection, and offers potential strategies to offload corresponding pathological effects, not only in WBSL but also in other aquaculture species.

Summary: Amphibians, like the paddy frog (Fejervarya multistriata), have played a critical role in the transition from water to land. Hibernation is a vital survival adaptation in cold environments with limited food resources. We decoded the paddy frog genome to reveal the molecular adaptations linked to hibernation in ectotherms. The genome contained 13 chromosomes, with a significant proportion of repetitive sequences. We identified the key genes encoding the proteins of AANAT, TRPM8, EGLN1, and VEGFA essential for circadian rhythms, thermosensation, and hypoxia during hibernation by comparing the hibernator and non-hibernator genomes. Examining organ changes during hibernation revealed the central regulatory role of the brain. We identified 21 factors contributing to hibernation, involving hormone biosynthesis, protein digestion, DNA replication, and the cell cycle. These findings provide deeper insight into the complex mechanisms of ectothermic hibernation and contribute to our understanding of the broader significance of this evolutionary adaptation.

Animals have evolved sophisticated temperature-sensing systems and mechanisms to detect and respond to ambient temperature changes. As a relict species endemic to the Qinghai-Tibet Plateau, hot-spring snake (Thermophis baileyi) survived the dramatic changes in climate that occurred during plateau uplift and ice ages, providing an excellent opportunity to explore the evolution of temperature sensation in ectotherms. Based on distributional information and behavioral experiments, we found that T. baileyi prefer hot-spring habitats and respond more quickly to warmth than other two snakes, suggesting that T. baileyi may evolve an efficient thermal-sensing system. Using high-quality chromosome-level assembly and comparative genomic analysis, we identified cold acclimation genes experiencing convergent acceleration in high-altitude lineages. We also discovered significant evolutionary changes in thermosensation- and thermoregulation-related genes, including the transient receptor potential (TRP) channels. Among these genes, TRPA1 exhibited three species-specific amino acid replacements, which differed from those found in infrared imaging snakes, implying different temperature-sensing molecular strategies. Based on laser-heating experiments, the T. baileyi-specific mutations in TRPA1 resulted in an increase in heat-induced opening probability and thermal sensitivity of the ion channels under the same degree of temperature stimulation, which may help the organism respond to temperature changes more quickly. These results provide insight into the genetic mechanisms underpinning the evolution of temperature-sensing strategies in ectotherms as well as genetic evidence of temperature acclimation in this group.