Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans
ABSTRACT Viruses play critical roles in shaping microbial distribution, organization, and ecological functions. However, the mechanisms behind the association and structuring of microbiomes with viruses still remain largely unknown. To understand how viruses affect the assembly of marine microbiomes...
Saved in:
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2025-07-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00539-25 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1839621709320159232 |
|---|---|
| author | Bo Wang Yantao Liang Kaiyue Lian Chuyu Zhang Meiaoxue Han Min Wang Hongbing Shao Andrew McMinn Hualong Wang |
| author_facet | Bo Wang Yantao Liang Kaiyue Lian Chuyu Zhang Meiaoxue Han Min Wang Hongbing Shao Andrew McMinn Hualong Wang |
| author_sort | Bo Wang |
| collection | DOAJ |
| description | ABSTRACT Viruses play critical roles in shaping microbial distribution, organization, and ecological functions. However, the mechanisms behind the association and structuring of microbiomes with viruses still remain largely unknown. To understand how viruses affect the assembly of marine microbiomes, the network complexity and stability of prokaryotic microbiomes with/without viruses were analyzed and compared using the Tara Ocean Project data set, including samples collected from the Indian Ocean (IO), South Pacific Ocean (SPO), North Pacific Ocean (NPO), Mediterranean Sea, and South Atlantic Ocean. The network complexity of prokaryotic communities was substantially different across oceans, being high in the IO and low in the SPO and NPO. Network complexity and stability of marine prokaryotic microbial communities were enhanced by the influence of viruses: microbiomes associated with viruses were more complex, had a high modularity, and were robust with low fragmentation and vulnerability and higher compositional stability than prokaryotic microbiomes without an association with viruses. Results presented here shed light on how the associations with viruses influenced microbial assembly and their co-occurrence pattern and stability across the oceans. Overall, given such changed environmental characteristics across the oceans, stable and resilient microbiome networks imply that biotic associations with viruses play a critical role in maintaining the integrity and resilience of marine microbiomes and their ecological functions.IMPORTANCEThis study represents the first detailed research on the effects of viruses on the organization of marine prokaryotic microbiomes at the global scale. Biotic factors and environmental heterogeneity directly and indirectly affect microbiome and viral co-occurrence with varied strength. Network complexity and stability of marine microbial communities were enhanced by the influence of viruses. Thus, given such dynamic environmental gradients in the ocean, stable and persistent microbiome networks suggest that biotic associations with viruses play a critical role in maintaining the integrity and resilience of marine microbiomes and influencing the function of marine ecosystems. |
| format | Article |
| id | doaj-art-711a08baad8b42daa5e65a91f97b6d21 |
| institution | Matheson Library |
| issn | 2379-5077 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj-art-711a08baad8b42daa5e65a91f97b6d212025-07-22T13:00:44ZengAmerican Society for MicrobiologymSystems2379-50772025-07-0110710.1128/msystems.00539-25Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceansBo Wang0Yantao Liang1Kaiyue Lian2Chuyu Zhang3Meiaoxue Han4Min Wang5Hongbing Shao6Andrew McMinn7Hualong Wang8College of Safety and Environmental Engineering, Shandong University of Science and Technology, Qingdao, Shandong, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaInstitute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, AustraliaUMT-OUC Joint Center for Marine Studies, Qingdao, ChinaABSTRACT Viruses play critical roles in shaping microbial distribution, organization, and ecological functions. However, the mechanisms behind the association and structuring of microbiomes with viruses still remain largely unknown. To understand how viruses affect the assembly of marine microbiomes, the network complexity and stability of prokaryotic microbiomes with/without viruses were analyzed and compared using the Tara Ocean Project data set, including samples collected from the Indian Ocean (IO), South Pacific Ocean (SPO), North Pacific Ocean (NPO), Mediterranean Sea, and South Atlantic Ocean. The network complexity of prokaryotic communities was substantially different across oceans, being high in the IO and low in the SPO and NPO. Network complexity and stability of marine prokaryotic microbial communities were enhanced by the influence of viruses: microbiomes associated with viruses were more complex, had a high modularity, and were robust with low fragmentation and vulnerability and higher compositional stability than prokaryotic microbiomes without an association with viruses. Results presented here shed light on how the associations with viruses influenced microbial assembly and their co-occurrence pattern and stability across the oceans. Overall, given such changed environmental characteristics across the oceans, stable and resilient microbiome networks imply that biotic associations with viruses play a critical role in maintaining the integrity and resilience of marine microbiomes and their ecological functions.IMPORTANCEThis study represents the first detailed research on the effects of viruses on the organization of marine prokaryotic microbiomes at the global scale. Biotic factors and environmental heterogeneity directly and indirectly affect microbiome and viral co-occurrence with varied strength. Network complexity and stability of marine microbial communities were enhanced by the influence of viruses. Thus, given such dynamic environmental gradients in the ocean, stable and persistent microbiome networks suggest that biotic associations with viruses play a critical role in maintaining the integrity and resilience of marine microbiomes and influencing the function of marine ecosystems.https://journals.asm.org/doi/10.1128/msystems.00539-25marine virusesprokaryotic microbiomesnetwork stabilitycommunity complexityenvironmental gradients |
| spellingShingle | Bo Wang Yantao Liang Kaiyue Lian Chuyu Zhang Meiaoxue Han Min Wang Hongbing Shao Andrew McMinn Hualong Wang Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans mSystems marine viruses prokaryotic microbiomes network stability community complexity environmental gradients |
| title | Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans |
| title_full | Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans |
| title_fullStr | Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans |
| title_full_unstemmed | Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans |
| title_short | Correlation with viruses enhances network complexity and stability of co-occurrence prokaryotes across the oceans |
| title_sort | correlation with viruses enhances network complexity and stability of co occurrence prokaryotes across the oceans |
| topic | marine viruses prokaryotic microbiomes network stability community complexity environmental gradients |
| url | https://journals.asm.org/doi/10.1128/msystems.00539-25 |
| work_keys_str_mv | AT bowang correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT yantaoliang correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT kaiyuelian correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT chuyuzhang correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT meiaoxuehan correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT minwang correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT hongbingshao correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT andrewmcminn correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans AT hualongwang correlationwithvirusesenhancesnetworkcomplexityandstabilityofcooccurrenceprokaryotesacrosstheoceans |