Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay
Abstract Background Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurr and how the inte...
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oai:doaj.org-article:9c649d0d05e74afaa38b1e6bc5f0b8db2021-11-28T12:23:46ZEstuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay10.1186/s40793-021-00392-z2524-6372https://doaj.org/article/9c649d0d05e74afaa38b1e6bc5f0b8db2021-11-01T00:00:00Zhttps://doi.org/10.1186/s40793-021-00392-zhttps://doaj.org/toc/2524-6372Abstract Background Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurr and how the inter-taxa networks respond to the strong environmental gradients in the estuaries. Results Here, we constructed co-occurrence networks on prokaryotic microbial communities in the CB, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks exhibited a clear seasonal pattern where microbes were more closely connected during warm season compared to the associations during cold season. In addition, microbial networks were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Multivariate regression tree (MRT) analysis and piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances along with nutrient availability, particulate carbon and Chl a, affected the distribution and co-occurrence of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia. Interestingly, compared to the abundant groups (such as SAR11, Saprospiraceae and Actinomarinaceae), the rare taxa including OM60 (NOR5) clade (Gammaproteobacteria), Micrococcales (Actinobacteria), and NS11-12 marine group (Bacteroidetes) contributed greatly to the stability of microbial co-occurrence in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences. Conclusion Our results shed light on how estuarine gradients alter the spatiotemporal variations of prokaryotic microbial networks in the estuarine ecosystem, as well as their adaptability to environmental disturbances and co-occurrence network complexity and stability.Hualong WangFeng ChenChuanlun ZhangMin WangJinjun KanBMCarticleEstuarine gradientsPlanktonic microbiomesCo-occurrenceNetwork stabilityChesapeake BayEnvironmental sciencesGE1-350MicrobiologyQR1-502ENEnvironmental Microbiome, Vol 16, Iss 1, Pp 1-18 (2021) |
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Estuarine gradients Planktonic microbiomes Co-occurrence Network stability Chesapeake Bay Environmental sciences GE1-350 Microbiology QR1-502 |
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Estuarine gradients Planktonic microbiomes Co-occurrence Network stability Chesapeake Bay Environmental sciences GE1-350 Microbiology QR1-502 Hualong Wang Feng Chen Chuanlun Zhang Min Wang Jinjun Kan Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
description |
Abstract Background Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurr and how the inter-taxa networks respond to the strong environmental gradients in the estuaries. Results Here, we constructed co-occurrence networks on prokaryotic microbial communities in the CB, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks exhibited a clear seasonal pattern where microbes were more closely connected during warm season compared to the associations during cold season. In addition, microbial networks were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Multivariate regression tree (MRT) analysis and piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances along with nutrient availability, particulate carbon and Chl a, affected the distribution and co-occurrence of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia. Interestingly, compared to the abundant groups (such as SAR11, Saprospiraceae and Actinomarinaceae), the rare taxa including OM60 (NOR5) clade (Gammaproteobacteria), Micrococcales (Actinobacteria), and NS11-12 marine group (Bacteroidetes) contributed greatly to the stability of microbial co-occurrence in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences. Conclusion Our results shed light on how estuarine gradients alter the spatiotemporal variations of prokaryotic microbial networks in the estuarine ecosystem, as well as their adaptability to environmental disturbances and co-occurrence network complexity and stability. |
format |
article |
author |
Hualong Wang Feng Chen Chuanlun Zhang Min Wang Jinjun Kan |
author_facet |
Hualong Wang Feng Chen Chuanlun Zhang Min Wang Jinjun Kan |
author_sort |
Hualong Wang |
title |
Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
title_short |
Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
title_full |
Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
title_fullStr |
Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
title_full_unstemmed |
Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay |
title_sort |
estuarine gradients dictate spatiotemporal variations of microbiome networks in the chesapeake bay |
publisher |
BMC |
publishDate |
2021 |
url |
https://doaj.org/article/9c649d0d05e74afaa38b1e6bc5f0b8db |
work_keys_str_mv |
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_version_ |
1718408031923863552 |