Decoupling of strain- and intrastrain-level interactions of microbiomes in a sponge holobiont

Wenxiu Wang, Weizhi Song, Marwan E. Majzoub, Xiaoyuan Feng, Bu Xu, Jianchang Tao, Yuanqing Zhu, Zhiyong Li, Pei-Yuan Qian, Nicole S. Webster, Torsten Thomas () and Lu Fan ()
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Wenxiu Wang: Southern University of Science and Technology
Weizhi Song: University of New South Wales
Marwan E. Majzoub: University of New South Wales
Xiaoyuan Feng: The Chinese University of Hong Kong
Bu Xu: Southern University of Science and Technology
Jianchang Tao: Southern University of Science and Technology
Yuanqing Zhu: Southern University of Science and Technology
Zhiyong Li: Shanghai Jiao Tong University
Pei-Yuan Qian: The Hong Kong University of Science and Technology
Nicole S. Webster: The Australian Antarctic Division
Torsten Thomas: University of New South Wales
Lu Fan: Southern University of Science and Technology

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Holobionts are highly organized assemblages of eukaryotic hosts, cellular microbial symbionts, and viruses, whose interactions and evolution involve complex biological processes. It is largely unknown which specific determinants drive similarity or individuality in genetic diversity between holobionts. Here, we combine short- and long-read sequencing and DNA-proximity-linkage technologies to investigate intraspecific diversity of the microbiomes, including host-resolved viruses, in individuals of a model marine sponge. We find strong impacts of the sponge host and the cellular hosts of viruses on strain-level organization of the holobiont, whereas substantial overlap in nucleotide diversity between holobionts suggests frequent exchanges of microbial cells and viruses at intrastrain level in the local sponge population. Immune-evasive arms races likely restricted virus-host co-evolution at the intrastrain level, generated holobiont-specific genome variations, and linked virus-host genetics through recombination. Our work shows that a decoupling of strain- and intrastrain-level interactions is a key factor in the genetic diversification of holobionts.

Date: 2024
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DOI: 10.1038/s41467-024-52464-6

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