Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China; Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang 641100, China.
Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China.
J Adv Res. 2024 Apr;58:93-104. doi: 10.1016/j.jare.2023.05.005. Epub 2023 May 21.
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.
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.
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.
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.
弹涂鱼是一类大型的两栖鱼类，它们发展出了许多形态和生理能力，以在陆地上生活。对三种有代表性的弹涂鱼，即大弹涂鱼（Boleophthalmus pectinirostris，BP）、大鳍鱚（Periophthalmus magnuspinnatus，PM）和小鳍鱚（P. modestus，PMO）的染色体水平基因组组装进行基因组比较，可能能够为水到陆的进化和适应提供新的见解。
通过PacBio、Nanopore 和 Hi-C 测序的整合，分别对 BP 和 PM 进行了两个染色体水平基因组的测序。随后对这两种弹涂鱼都进行了一系列标准的组装和注释流程。我们还重新注释了从 NCBI 下载的 PMO 基因组，以获得冗余减少的注释。在大规模上对这三种弹涂鱼的基因组进行了三向比较分析，以发现基因大小等详细的基因组差异，以及潜在的染色体分裂和融合事件。还比较了三种两栖弹涂鱼和其他一些硬骨鱼的几个代表性基因家族，以找到一些陆地适应的分子线索。
我们获得了两个高质量的单倍型基因组组装，BP 的基因组有 23 条染色体，PM 的基因组有 25 条染色体。我们还在 PM 中发现了两个特定的染色体分裂事件。祖先染色体分析发现了弹涂鱼祖先的一次共同融合事件。这个融合事件随后在所有三种弹涂鱼物种中都被保留下来。在三种弹涂鱼的基因组中，发现了一些 SCPP（分泌型钙结合磷酸蛋白）基因的缺失，这可能导致部分时间在陆地上生活的鱼类鳞片减少。PM 中的 aanat1a 基因（编码多巴胺代谢和褪黑素生物合成的重要酶，即芳香烷基胺 N-乙酰转移酶 1a，AANAT1a）缺失已得到证实，但 PMO 中没有缺失（如之前在 BP 中报道的存在），这表明 PM 的空气视觉比 PMO 和 BP 都要好。这种属内的微小差异足以证明弹涂鱼的水到陆的适应是一个逐步进化的过程。
这些高质量的弹涂鱼基因组组装将成为深入发现两栖鱼类陆地适应的基因组进化的宝贵遗传资源。
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