Symbiotic microbiome and metabolism profiles reveal the effects of induction by oysters on the metamorphosis of the carnivorous gastropod Rapana venosa

Mei-Jie Yang; Hao Song; Jie Feng; Zheng-Lin Yu; Pu Shi; Jian Liang; Zhi Hu; Cong Zhou; Xiao-Lin Wang; Tao Zhang

doi:10.1016/j.csbj.2021.11.041

Symbiotic microbiome and metabolism profiles reveal the effects of induction by oysters on the metamorphosis of the carnivorous gastropod Rapana venosa

Comput Struct Biotechnol J. 2021 Dec 4:20:1-14. doi: 10.1016/j.csbj.2021.11.041. eCollection 2022.

Authors

Mei-Jie Yang^{1

2

3

4

5}, Hao Song^{1

2

3

4}, Jie Feng^{1

2

3

4}, Zheng-Lin Yu^{1

2

3

4}, Pu Shi^{1

2

3

4

5}, Jian Liang⁶, Zhi Hu^{1

2

3

4

5}, Cong Zhou^{1

2

3

4

5}, Xiao-Lin Wang^{1

2

3

4}, Tao Zhang^{1

2

3

4

7}

Affiliations

¹ CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.
² Laboratory for Marine Science and Technology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.
³ Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China.
⁴ CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.
⁵ University of Chinese Academy of Sciences, Beijing, China.
⁶ Tianjin Key Laboratory of Aqua-ecology and Aquaculture, Fisheries College, Tianjin Agricultural University, Tianjin 300384, China.
⁷ Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, China.

Abstract

Most marine mollusks have a pelagic larval phase, and they need to undergo metamorphosis to develop into adults. Metamorphosis is affected by many factors, including abiotic factors such as temperature, salinity and illumination as well as biological factors such as food and microorganisms. In our previous study, we found that the metamorphosis of Rapana venosa requires induction by juvenile oysters, which are the food source of R. venosa. However, the regulatory mechanism of this induction is largely unknown. In the present study, we evaluated the impacts of induction by juvenile oysters on competent larvae of R. venosa. Competent larvae were experimentally divided into two pools, and scallop shells without juvenile oysters and scallop shells with juvenile oysters were added for 2 h and 12 h to monitor alterations in critical gene expression, symbiotic microbiota and metabolomic responses. The carboxypeptidase gene was increased while the cellulase gene was decreased, which may mean that the food habit transition was induced by juvenile oysters. Meanwhile, critical genes in the neuroendocrine system were also significantly altered in juvenile oysters. Furthermore, dramatic changes in the symbiotic microbiota and metabolism profiles were observed, with many of them associated with the digestive system and neuroendocrine system. In conclusion, juveniles as food resources may induce metamorphosis in R. venosa by regulating the neuroendocrine system and promoting the development of the digestive system and changes in digestive enzymes. This study may provide evidence that induction by juvenile oysters can promote food habit transition and metamorphosis in R. venosa by regulating the metabolome and microbiome and further altering the digestive and neuroendocrine systems of R. venosa, which expands our understanding of the regulatory mechanism of metamorphosis in R. venosa. However, further studies are needed to explore the specific substance inducing metamorphosis released by juvenile oysters.

Keywords: Digestive system; Metabolism profiles; Metamorphosis; Neuroendocrine system; Symbiotic microbiota.