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Abstract Global warming has threatened all-rounded hierarchical biosphere by reconstructing eco-structure and bringing biodiversity variations. Pacific white shrimp, a successful model of worldwide utilizing marine ectothermic resources, is facing huge losses due to multiple diseases relevant to intestinal microbiota (IM) dysbiosis during temperature fluctuation. However, how warming mediates shrimp health remains poorly understood. Herein, a global shrimp IM catalogue was conducted via 1,369 shrimp IM data from nine countries, including 918 samples from previously published data and 451 generated in the study. Shrimp IMs were stratified into three enterotypes with distinctive compositions and functions, dominated by Vibrio, Shewanella and Candidatus Bacilloplasma, which showed an obvious distribution bias between enterotypes and diseases. The ratio of Vibrio and Candidatus Bacilloplasma was a crucial indicator for shrimp health. Moreover, temperature was the most driving factor for microbial composition, which potentially led to the migration of enterotypes, and high probability of white feces syndrome and low risk of hepatopancreas necrosis syndrome. Collectively, the warming-driven enterotypes mediated shrimp health, which exemplified the causal relationship between temperature rising and ectothermic animals’ health. These findings enlarged the cognition of shrimp health culture management from a microecological perspective, and alerted the inevitable challenge of global warming to ectothermic animals.

Symbiotic gut bacteria play crucial role in host health. Symbionts are widely distributed in arthropod intestines, but their ecological functions are poorly understood due to the inability to cultivate them. Members of Candidatus Bacilliplasma (CB) are widely distributed in crustacean intestine and maybe commensals with hosts, but the paucity of pure cultures has limited further insights into their physiologies and functions. Here, four strains of representative CB bacteria in shrimp intestine were successfully isolated and identified as members of a novel Order in the Phylum Mycoplasmatota. Through genome assembly, the circular genome maps of the four strains were obtained, and the number of coding genes ranged from 1,886 to 1,980. Genomic analysis suggested that the bacteria were missing genes for many critical pathways including the TCA cycle and biosynthesis pathways for amino acids and coenzyme factors. The analysis of 16S amplification data showed that Shewanella, Pseudomonas and CB were the dominant at the genera level in the intestine of Penaeus vannamei. Ecological functional experiments revealed that the strains were symbionts and colonized shrimp intestines. Our valued findings can greatly enhance our understanding and provides new insights into the potentially significant role of uncultured symbiotic bacteria in modulating host health.

Emerging evidence supports that the phage-prokaryote interaction drives ecological processes in various environments with different phage life strategies. However, the knowledge of phage-prokaryote interaction in the shrimp culture pond ecosystem (SCPE) is still limited. Here, the viral and prokaryotic community profiles at four culture stages in the intestine of Litopenaeus vannamei and cultural sediment microhabitats of SCPE were explored to elucidate the contribution of phage-prokaryote interaction in modulating microbial communities. The results demonstrated that the most abundant viral families in the shrimp intestine and sediment were Microviridae, Circoviridae, Inoviridae, Siphoviridae, Podoviridae, Myoviridae, Parvoviridae, Herelleviridae, Mimiviridae, and Genomoviridae, while phages dominated the viral community. The dominant prokaryotic genera were Vibrio, Formosa, Aurantisolimonas, and Shewanella in the shrimp intestine, and Formosa, Aurantisolimonas, Algoriphagus, and Flavobacterium in the sediment. The viral and prokaryotic composition of the shrimp intestine and sediment were significantly different at four culture stages, and the phage communities were closely related to the prokaryotic communities. Moreover, the phage-prokaryote interactions can directly or indirectly modulate the microbial community composition and function, including auxiliary metabolic genes and closed toxin genes. The interactional analysis revealed that phages and prokaryotes had diverse coexistence strategies in the shrimp intestine and sediment microhabitats of SCPE. Collectively, our findings characterized the composition of viral communities in the shrimp intestine and cultural sediment and revealed the distinct pattern of phage-prokaryote interaction in modulating microbial community diversity, which expanded our cognization of the phage-prokaryote coexistence strategy in aquatic ecosystems from the microecological perspective and provided theoretical support for microecological prevention and control of shrimp culture health management.