Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay

ABSTRACT Eutrophication occurring in coastal bays is prominent in impacting local ecosystem structure and functioning. To understand how coastal bay ecosystem function responds to eutrophication, comprehending the ecological processes associated with microbial community assembly is critical. However...

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Main Authors: Huajun Zhang, Yi Yan, Tenghui Lin, Weijuan Xie, Jian Hu, Fanrong Hou, Qingxi Han, Xiangyu Zhu, Demin Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01481-22
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author Huajun Zhang
Yi Yan
Tenghui Lin
Weijuan Xie
Jian Hu
Fanrong Hou
Qingxi Han
Xiangyu Zhu
Demin Zhang
author_facet Huajun Zhang
Yi Yan
Tenghui Lin
Weijuan Xie
Jian Hu
Fanrong Hou
Qingxi Han
Xiangyu Zhu
Demin Zhang
author_sort Huajun Zhang
collection DOAJ
description ABSTRACT Eutrophication occurring in coastal bays is prominent in impacting local ecosystem structure and functioning. To understand how coastal bay ecosystem function responds to eutrophication, comprehending the ecological processes associated with microbial community assembly is critical. However, quantifying the contribution of ecological processes to the assembly of prokaryotic communities is still limited in eutrophic waters. Moreover, the influence of these ecological processes on microbial interactions is poorly understood. Here, we examined the assembly processes and co-occurrence patterns of prokaryotic communities in a eutrophic bay using 156 surface seawater samples collected over 12 months. The variation of prokaryotic community compositions (PCCs) could be mainly explained by environmental factors, of which temperature was the most important. Under high environmental heterogeneity conditions in low-temperature seasons, heterogeneous selection was the major assembly process, resulting in high β-diversity and more tightly connected co-occurrence networks. When environmental heterogeneity decreased in high-temperature seasons, drift took over, leading to decline in β-diversity and network associations. Microeukaryotes were found to be important biological factors affecting PCCs. Our results first disentangled the contribution of drift and microbial interactions to the large unexplained variation of prokaryotic communities in eutrophic waters. Furthermore, a new conceptual model linking microbial interactions to ecological processes was proposed under different environmental heterogeneity. Overall, our study sheds new light on the relationship between assembly processes and co-occurrence of prokaryotic communities in eutrophic waters. IMPORTANCE A growing number of studies have examined roles of microbial community assembly in modulating community composition. However, the relationships between community assembly and microbial interactions are not fully understood and rarely tested, especially in eutrophic waters. In this study, we built a conceptual model that links seasonal microbial interactions to ecological processes, which has not been reported before. The model showed that heterogeneous selection plays an important role in driving community assembly during low-temperature seasons, resulting in higher β-diversity and more tightly connected networks. In contrast, drift became a dominant force during high-temperature seasons, leading to declines in the β-diversity and network associations. This model could function as a new framework to predict how prokaryotic communities respond to intensified eutrophication induced by climate change in coastal environment.
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spelling doaj.art-ef7954a1ef9042619b747817ac7d81a42022-12-22T00:33:12ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.01481-22Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic BayHuajun Zhang0Yi Yan1Tenghui Lin2Weijuan Xie3Jian Hu4Fanrong Hou5Qingxi Han6Xiangyu Zhu7Demin Zhang8State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaKey Laboratory of Applied Marine Biotechnology of Department of Education, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaKey Laboratory of Applied Marine Biotechnology of Department of Education, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaEnvironmental Monitoring Center of Ningbo, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaABSTRACT Eutrophication occurring in coastal bays is prominent in impacting local ecosystem structure and functioning. To understand how coastal bay ecosystem function responds to eutrophication, comprehending the ecological processes associated with microbial community assembly is critical. However, quantifying the contribution of ecological processes to the assembly of prokaryotic communities is still limited in eutrophic waters. Moreover, the influence of these ecological processes on microbial interactions is poorly understood. Here, we examined the assembly processes and co-occurrence patterns of prokaryotic communities in a eutrophic bay using 156 surface seawater samples collected over 12 months. The variation of prokaryotic community compositions (PCCs) could be mainly explained by environmental factors, of which temperature was the most important. Under high environmental heterogeneity conditions in low-temperature seasons, heterogeneous selection was the major assembly process, resulting in high β-diversity and more tightly connected co-occurrence networks. When environmental heterogeneity decreased in high-temperature seasons, drift took over, leading to decline in β-diversity and network associations. Microeukaryotes were found to be important biological factors affecting PCCs. Our results first disentangled the contribution of drift and microbial interactions to the large unexplained variation of prokaryotic communities in eutrophic waters. Furthermore, a new conceptual model linking microbial interactions to ecological processes was proposed under different environmental heterogeneity. Overall, our study sheds new light on the relationship between assembly processes and co-occurrence of prokaryotic communities in eutrophic waters. IMPORTANCE A growing number of studies have examined roles of microbial community assembly in modulating community composition. However, the relationships between community assembly and microbial interactions are not fully understood and rarely tested, especially in eutrophic waters. In this study, we built a conceptual model that links seasonal microbial interactions to ecological processes, which has not been reported before. The model showed that heterogeneous selection plays an important role in driving community assembly during low-temperature seasons, resulting in higher β-diversity and more tightly connected networks. In contrast, drift became a dominant force during high-temperature seasons, leading to declines in the β-diversity and network associations. This model could function as a new framework to predict how prokaryotic communities respond to intensified eutrophication induced by climate change in coastal environment.https://journals.asm.org/doi/10.1128/spectrum.01481-22temperaturecommunity assemblyco-occurrence networksprokaryotic communitiesXiangshan Bay
spellingShingle Huajun Zhang
Yi Yan
Tenghui Lin
Weijuan Xie
Jian Hu
Fanrong Hou
Qingxi Han
Xiangyu Zhu
Demin Zhang
Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
Microbiology Spectrum
temperature
community assembly
co-occurrence networks
prokaryotic communities
Xiangshan Bay
title Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
title_full Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
title_fullStr Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
title_full_unstemmed Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
title_short Disentangling the Mechanisms Shaping the Prokaryotic Communities in a Eutrophic Bay
title_sort disentangling the mechanisms shaping the prokaryotic communities in a eutrophic bay
topic temperature
community assembly
co-occurrence networks
prokaryotic communities
Xiangshan Bay
url https://journals.asm.org/doi/10.1128/spectrum.01481-22
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