Taxonomic composition and functional potentials of gastrointestinal microbiota in 12 wild-stranded cetaceans

Jie Fan; Hui Kang; Meiqi Lv; Yuhuan Zhai; Yangyang Jia; Zixin Yang; Chengcheng Shi; Changhao Zhou; Lin Diao; Jingsuo Li; Xiaowei Jin; Shanshan Liu; Karsten Kristiansen; Peijun Zhang; Jianwei Chen; Songhai Li

doi:10.3389/fmicb.2024.1394745

Taxonomic composition and functional potentials of gastrointestinal microbiota in 12 wild-stranded cetaceans

Front Microbiol. 2024 Aug 29:15:1394745. doi: 10.3389/fmicb.2024.1394745. eCollection 2024.

Authors

Jie Fan^#^{1

2}, Hui Kang^#^{1

3}, Meiqi Lv^#², Yuhuan Zhai^{1

3}, Yangyang Jia⁴, Zixin Yang³, Chengcheng Shi², Changhao Zhou², Lin Diao², Jingsuo Li², Xiaowei Jin⁵, Shanshan Liu², Karsten Kristiansen^{6

7}, Peijun Zhang³, Jianwei Chen^{2

6

7}, Songhai Li^{3

8}

Affiliations

¹ College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China.
² BGI Research, Qingdao, China.
³ Marine Mammal and Marine Bioacoustics Laboratory, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, China.
⁴ BGI Research, Shenzhen, China.
⁵ China National Environmental Monitoring Centre, Beijing, China.
⁶ Qingdao Key Laboratory of Marine Genomics, and Qingdao-Europe Advanced Institute for Life Sciences, BGI Research, Qingdao, China.
⁷ Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
⁸ The Innovation Research Center for Aquatic Mammals, and Key Laboratory of Aquatic Biodiversity and Conservation of the Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.

^# Contributed equally.

Abstract

Cetaceans play a crucial role in marine ecosystems; however, research on their gastrointestinal microbiota remains limited due to sampling constraints. In this study, we collected hindgut samples from 12 stranded cetaceans and performed 16S rRNA gene amplicon sequencing to investigate microbial composition and functional potentials. Analysis of ZOTUs profiles revealed that the phyla Firmicutes, Proteobacteria, and Bacteroidetes dominated all hindgut samples. However, unique microbial profiles were observed among different cetacean species, with significant separation of gut microbiota communities according to biological evolutionary lineages. Different genera that contain pathogens were observed distinguishing delphinids from physeteroids/ziphiids. Delphinid samples exhibited higher abundances of Vibrio, Escherichia, and Paeniclostridium, whereas physeteroid and ziphiid samples showed higher abundances of Pseudomonas, Enterococcus, and Intestinimonas. Functional analysis indicated convergence in the gut microbiota among all cetaceans, with shared bacterial infection pathways across hindgut samples. In addition, a comparison of the gastrointestinal microbial composition between a stranded short-finned pilot whale (Globicephala macrorhynchus) and a stranded rough-toothed dolphin (Steno bredanensis) using 16S rRNA gene sequencing revealed distinct microbial community structures and functional capacities. To the best of our knowledge, this study represents the first report on the gastrointestinal microbiota of the pantropical spotted dolphin (Stenella attenuata), Blainville's beaked whale (Mesoplodon densirostris), and rough-toothed dolphin, with various comparisons conducted among different cetacean species. Our findings enhance the understanding of microbial composition and diversity in cetacean gastrointestinal microbiota, providing new insights into co-evolution and complex interactions between cetacean microbes and hosts.

Keywords: delphinids; food digestion; functional potentials; gastrointestinal microbiota; gut microbiota; physeteroids and ziphiid; stranded cetaceans.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was partly supported by the National Key R&D Program of China (Grant Nos. 2022YFF1301601, 2021YFC2800304, and 2021YFC2800403), the Joint Funds of the National Natural Science Foundation of China (Grant No. U2106228), the National Natural Science Foundation of China (Grant No. 32100047), the “One Belt and One Road” Science and Technology Cooperation Special Program of the International Partnership Program of the Chinese Academy of Sciences (Grant No. 183446KYSB20200016), and the Hainan Provincial Natural Science Foundation of China (Grant No. 422RC744).