Changes in community structures and functions of the gut microbiomes of deep-sea cold seep mussels during in situ transplantation experiment

Animal Microbiome · 12 authors, 5 centres

AI SUMMARY

FIDELITY 92%

POPULATIONDeep-sea cold seep mussels (Gigantidas haimaensis) from the Haima cold seep, South China Sea

INTERVENTIONIn situ transplantation of mussels from a dense mussel bed to a peripheral site 100 m away for 6 days

COMPARISONMussels at the original site vs. mussels after transplantation to the peripheral site

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AGENT 01 · STRUCTURED SUMMARY

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TL;DR

This study provides the first metagenomic analysis of gut microbiomes in deep-sea cold seep mussels (Gigantidas haimaensis). Using an in situ transplantation experiment, the authors show that the gut microbiome shifts in response to environmental change, with Gammaproteobacteria becoming enriched and Bacteroidetes depleted, and that these changes help the mussels adapt to altered methane, ammonia, and sulphide availability. The findings reveal that the gut microbiome plays a critical nutritional and adaptive role in deep-sea chemosymbiotic mussels, complementing the function of gill symbionts.

Full summary

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**Background:** Deep-sea cold seep mussels rely on chemoautotrophic symbionts in their gills for nutrition, but they also retain a functional digestive system. The role of the gut microbiome in these mussels, particularly under environmental change, is poorly understood. This study investigates the community structure and functional capabilities of the gut microbiome in the cold seep mussel *Gigantidas haimaensis* and how it responds to environmental shifts.

**Methods:** Mussels were collected from a dense mussel bed at the Haima cold seep (~1400 m depth, South China Sea) using the ROV *Haima 2*. A subset was transplanted 100 m away to a peripheral site with no mussels for 6 days (May 2021). After in situ fixation in RNA stabilizing solution, eight mussel specimens (four from each site) were dissected into stomach, GI segment I, and GI segment II. DNA was extracted and subjected to 16S rRNA gene amplicon sequencing (V3–V4, Illumina NovaSeq-PE250) and metagenomic sequencing (Illumina NovaSeq 6000, ~10 Gb per tissue). Taxonomic profiling used Kaiju v1.8.2 against NCBI RefSeq. Alpha diversity (ACE, Chao1, Richness, Shannon, Simpson) and beta diversity (Bray–Curtis, nMDS) were calculated from rarefied ASV tables (4000 reads/sample) using QIIME2 and vegan. Metagenomic contigs were assembled with SPAdes, and bacterial contigs were annotated against NR, COG, KEGG (GhostKOALA), Pfam, and dbCAN databases. Fisher’s exact test with Bonferroni correction identified significantly influenced KEGG orthologs. Histology (HE staining) and FISH (probes EUB338-FITC, Alf968-Cy3, Gamma42a-Cy5) were performed on gut sections.

**Key Results:** At the original site, *Proteobacteria* was the most abundant phylum, with *Alphaproteobacteria* dominating (average 33.65%) followed by *Gammaproteobacteria* (average 21.9%). After transplantation, *Proteobacteria* increased from 68.06% to 73.23% on average, and *Gammaproteobacteria* became the dominant class in all tissues, while *Bacteroidetes* declined. Alpha diversity indices (ACE, Chao1, Richness) decreased significantly (p < 0.05) in the transplantation group. nMDS showed significant community separation (ANOSIM r = 0.2711, p = 0.012). Only 572 of 5,033 ASVs (11.4%) overlapped between groups. Functional analysis identified 2,113 CAZyme hits (153 types), with 41% from *Bacteroides* (116 types). After transplantation, CAZyme categories decreased from 153 to 60. Positively influenced KEGG pathways included starch and sucrose metabolism (disaccharide breakdown), nitrite reductase (nirB) increase, and glutamate dehydrogenase (gdhA) decrease. Environmental ammonium was 23.8 mg/L at the original site and 37.4 mg/L at the transplantation site; sulphide was 0.13 mg/L and 0.8 mg/L, respectively. Thiosulphate reductase decreased after transplantation. Lantibiotic biosynthesis protein (NisB), sporulation sensor kinase B (kinB), and chemotaxis proteins (CheR, CheB) increased in the transplantation group. The type VI secretion system (T6SS) and Rhs-family toxins were identified, indicating interbacterial competition. FISH confirmed bacterial populations in GI segment I contents.

**Clinical Implications:** While not a clinical study, this research provides fundamental insights into host–microbiome interactions in extreme environments. Understanding how gut microbiomes adapt to environmental stressors (e.g., reduced methane, altered nitrogen/sulphur availability) has implications for predicting the resilience of deep-sea ecosystems to environmental change, including anthropogenic disturbances and climate-driven shifts in chemosynthetic habitats. The findings also contribute to the broader understanding of mixotrophic nutrition and microbial adaptation in animals with reduced symbiont function.

PICO

PPOPULATION

Deep-sea cold seep mussels (Gigantidas haimaensis) from the Haima cold seep, South China Sea

IINTERVENTION

In situ transplantation of mussels from a dense mussel bed to a peripheral site 100 m away for 6 days

OOUTCOME

Changes in gut microbiome community structure (16S rRNA amplicon and metagenomic sequencing), alpha and beta diversity, functional gene profiles (KEGG, COG, CAZyme), and histology/FISH analysis

STUDY TYPE

other

SPECIALTY

microbiology

SUMMARISED BY

AI pipeline

FIDELITY CHECK

92% · A

ORIGINAL PAPER

PMC10008618

Changes in community structures and functions of the gut microbiomes of deep-sea cold seep mussels during in situ transplantation experiment

Animal Microbiome

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ABSTRACT

Abstract Background Many deep-sea invertebrates largely depend on chemoautotrophic symbionts for energy and nutrition, and some of them have reduced functional digestive tracts. By contrast, deep-sea mussels have a complete digestive system although symbionts in their gills play vital roles in nutrient supply. This digestive system remains functional and can utilise available resources, but the roles and associations among gut microbiomes in these mussels remain unknown. Specifically, how the gut microbiome reacts to environmental change is unclear. Results The meta-pathway analysis showed the nutritional and metabolic roles of the deep-sea mussel gut microbiome. Comparative analyses of the gut microbiomes of original and transplanted mussels subjected to environmental change revealed shifts in bacterial communities. Gammaproteobacteria were enriched, whereas Bacteroidetes were slightly depleted. The functional response for the shifted communities was attributed to the acquisition of carbon sources and adjusting the utilisation of ammonia and sulphide. Self-protection was observed after transplantation. Conclusion This study provides the first metagenomic insights into the community structure and function of the gut microbiome in deep-sea chemosymbiotic mussels and their critical mechanisms for adapting to changing environments and meeting of essential nutrient demand. Supplementary Information The online version contains supplementary material available at 10.1186/s42523-023-00238-8. Keywords: Gigantidas mussel, Metagenome, Nutritional role, Haima seep, In situ experiment

CITATION EXPORT

Yao Xiao, Hao Wang, Yi Lan et al.. Changes in community structures and functions of the gut microbiomes of deep-sea cold seep mussels during in situ transplantation experiment. Animal Microbiome. (2023). https://doi.org/10.1186/s42523-023-00238-8

AUTHORS

12 · 5 CENTRES

Yao Xiao, Hao Wang, Yi Lan, Cheng Zhong, Guoyong Yan, Zhimeng Xu, Guangyuan Lu, Jiawei Chen, Tong Wei, Wai Chuen Wong, Yick Hang Kwan, Pei-Yuan Qian

1Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458 People’s Republic of China
2Department of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong, People’s Republic of China
3Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, People’s Republic of China
4Research Center for the Oceans and Human Health, City University of Hong Kong Shenzhen Research Institute, Shenzhen, 51807 People’s Republic of China
5Department of Biology, HADAL and Nordcee, University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark