Population genomics, gut microbiota, and transcriptional response to heat shock in Hong Kong oyster Magallana hongkongensis

The Hong Kong oyster Magallana hongkongensis, previously known as Crassostrea hongkongensis, is a true oyster species that native to the estuary-coast of Pearl River Delta in southern China. The species has long been farmed for hundreds of years, and with scientific, ecological, cultural and nutritional importance. However, there is only limited information on the genetic background and stress adaptation mechanism of M. hongkongensis, restricting the sustainable production and utilisation of the local oyster resources. Here, we presented the population structure analysis on oysters collected from Deep Bay (Shenzhen Bay) and Lantau Island in Hong Kong, the transcriptome analysis on heat shock responses and the gut microbiota profile of M. hongkongensis. A conserved genetic background of local oysters was uncovered by the whole genome resequencing on 49 individuals, and the results indicated a close relationship and adaptation process in local oyster populations. Genetic variants in homeobox and heat shock protein genes were identified and predicted with regulatory function. Oysters had also been incubated under temperate (25 °C) and heat shock (32 °C) conditions for 24 hours to investigate the stress responses. Transcriptome profiles revealed the heat-induced regulation on heat shock protein, protein binding genes and signal transduction genes. We also found the differential expression of two splicing factors might be regulated by alternative splicing, and their expression levels were higher under heat stress. In addition, the gut microbe community were detected by 16S rRNA sequencing, and Cyanobacteria, Proteobacteria and Spirochaetes were the top phyla found in local oysters. Our results provided the knowledge on transcriptomic responses to heat shock in local oyster and implied the molecular basis for the divergent adaptation to the changeable aquatic environment. We also suggested that gut microbiota might participate in the regulation of stress response in M. hongkongensis. These findings give new insights on different mechanisms of local adaptation in Hong Kong oysters and other molluscs.

香港牡蛎（Magallana hongkongensis），曾用名Crassostrea hongkongensis，是原生分布于中国南部珠江三角洲河口海岸的真牡蛎物种。该物种已有数百年的养殖历史，兼具科学、生态、文化与营养价值。然而，目前关于香港牡蛎的遗传背景与胁迫适应机制的研究信息较为有限，制约了这一本地牡蛎资源的可持续生产与利用。本研究对采自香港后海湾（深圳湾）与大屿山的牡蛎样本开展了群体结构分析（population structure analysis），同时完成了香港牡蛎的热激响应转录组（transcriptome）分析与肠道微生物组特征解析。通过对49个个体进行全基因组重测序（whole genome resequencing），我们揭示了本地牡蛎的保守遗传背景，结果显示本地牡蛎种群间亲缘关系紧密且存在共同的适应过程。研究鉴定了同源框基因与热休克蛋白（heat shock protein）基因的遗传变异，并预测其具有调控功能。我们将牡蛎分别置于适温（25℃）与热激（32℃）环境中培养24小时，以探究其胁迫响应。转录组分析结果显示，热激可调控热休克蛋白、蛋白结合基因以及信号转导基因的表达。此外，我们发现两种剪接因子的差异表达可能受可变剪接（alternative splicing）调控，且在热胁迫条件下其表达水平更高。本研究还通过16S rRNA测序（16S rRNA sequencing）检测了肠道微生物群落，发现蓝细菌门（Cyanobacteria）、变形菌门（Proteobacteria）与螺旋体门（Spirochaetes）为本地牡蛎中的优势菌门。本研究结果为解析本地牡蛎的热激转录响应提供了理论基础，并揭示了其应对多变水生环境的适应性分子机制。同时，我们提出肠道微生物组可能参与调控香港牡蛎的胁迫响应过程。上述发现为香港牡蛎及其他软体动物的本地适应机制研究提供了新的视角。