Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism

ABSTRACT Marine phytoplankton and heterotrophic bacteria share a very close but usually changeable relationship. However, the ultimate fate of their unstable relationship on a long-term scale is unclear. Here, the relationship between Synechococcus and heterotrophic bacterial communities underwent a...

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Autores principales: Zenghu Zhang, Shailesh Nair, Lili Tang, Hanshuang Zhao, Zhenzhen Hu, Mingming Chen, Yao Zhang, Shuh-Ji Kao, Nianzhi Jiao, Yongyu Zhang
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:4f13284c974441edae91de7af422fe4d2021-11-10T18:37:51ZLong-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism10.1128/mBio.01614-212150-7511https://doaj.org/article/4f13284c974441edae91de7af422fe4d2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01614-21https://doaj.org/toc/2150-7511ABSTRACT Marine phytoplankton and heterotrophic bacteria share a very close but usually changeable relationship. However, the ultimate fate of their unstable relationship on a long-term scale is unclear. Here, the relationship between Synechococcus and heterotrophic bacterial communities underwent a dramatic shift from antagonism to commensalism and eventually to mutualism during long-term cocultivation. The relationship change is attributed to the different (even opposite) effects of diverse bacterial members on Synechococcus and the ratio of beneficial to harmful bacteria. Different bacterial members also interact with each other (e.g., quorum-sensing communication, hostility, or mutual promotion) and drive a dynamic succession in the entire community structure that corresponds exactly to the shift in its relationship with Synechococcus. In the final mutualism stage, a self-sufficient nitrogen cycle, including nitrogen fixation, denitrification, and organic nitrogen degradation, contributed to the healthy survival of Synechococcus for 2 years without an exogenous nutrient supply. This natural selective trait of Synechococcus and heterotrophic bacteria toward mutualism under long-term coexistence provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans. IMPORTANCE Phytoplankton and heterotrophic bacteria have a close but usually changeable relationship. Uncovering the dynamic changes and driving factors of their interrelationships is of great significance for an in-depth understanding of the ecological processes and functions of marine microorganisms. Here, we observed that Synechococcus and heterotrophic bacterial communities underwent a dramatic change in their relationship from antagonism to mutualism during a long-term cocultivation process. We revealed that the interactions between different members of the bacterial community and the combined effects of different bacterial individuals on Synechococcus promoted the dynamic changes of the Synechococcus-bacterium relationship. In the end, a self-sufficient nutrient cycle (especially nitrogen) established by Synechococcus and bacterial communities supported their long-term survival without any external nutrition supply. This study provides novel insight into the interaction between Synechococcus and heterotrophic bacteria in the ocean and provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans.Zenghu ZhangShailesh NairLili TangHanshuang ZhaoZhenzhen HuMingming ChenYao ZhangShuh-Ji KaoNianzhi JiaoYongyu ZhangAmerican Society for MicrobiologyarticleSynechococcusheterotrophic bacterial communityalgae-bacteria interactionmutualismnitrogen cycleMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution DOAJ
collection DOAJ
language EN
topic Synechococcus
heterotrophic bacterial community
algae-bacteria interaction
mutualism
nitrogen cycle
Microbiology
QR1-502
spellingShingle Synechococcus
heterotrophic bacterial community
algae-bacteria interaction
mutualism
nitrogen cycle
Microbiology
QR1-502
Zenghu Zhang
Shailesh Nair
Lili Tang
Hanshuang Zhao
Zhenzhen Hu
Mingming Chen
Yao Zhang
Shuh-Ji Kao
Nianzhi Jiao
Yongyu Zhang
Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
description ABSTRACT Marine phytoplankton and heterotrophic bacteria share a very close but usually changeable relationship. However, the ultimate fate of their unstable relationship on a long-term scale is unclear. Here, the relationship between Synechococcus and heterotrophic bacterial communities underwent a dramatic shift from antagonism to commensalism and eventually to mutualism during long-term cocultivation. The relationship change is attributed to the different (even opposite) effects of diverse bacterial members on Synechococcus and the ratio of beneficial to harmful bacteria. Different bacterial members also interact with each other (e.g., quorum-sensing communication, hostility, or mutual promotion) and drive a dynamic succession in the entire community structure that corresponds exactly to the shift in its relationship with Synechococcus. In the final mutualism stage, a self-sufficient nitrogen cycle, including nitrogen fixation, denitrification, and organic nitrogen degradation, contributed to the healthy survival of Synechococcus for 2 years without an exogenous nutrient supply. This natural selective trait of Synechococcus and heterotrophic bacteria toward mutualism under long-term coexistence provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans. IMPORTANCE Phytoplankton and heterotrophic bacteria have a close but usually changeable relationship. Uncovering the dynamic changes and driving factors of their interrelationships is of great significance for an in-depth understanding of the ecological processes and functions of marine microorganisms. Here, we observed that Synechococcus and heterotrophic bacterial communities underwent a dramatic change in their relationship from antagonism to mutualism during a long-term cocultivation process. We revealed that the interactions between different members of the bacterial community and the combined effects of different bacterial individuals on Synechococcus promoted the dynamic changes of the Synechococcus-bacterium relationship. In the end, a self-sufficient nutrient cycle (especially nitrogen) established by Synechococcus and bacterial communities supported their long-term survival without any external nutrition supply. This study provides novel insight into the interaction between Synechococcus and heterotrophic bacteria in the ocean and provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans.
format article
author Zenghu Zhang
Shailesh Nair
Lili Tang
Hanshuang Zhao
Zhenzhen Hu
Mingming Chen
Yao Zhang
Shuh-Ji Kao
Nianzhi Jiao
Yongyu Zhang
author_facet Zenghu Zhang
Shailesh Nair
Lili Tang
Hanshuang Zhao
Zhenzhen Hu
Mingming Chen
Yao Zhang
Shuh-Ji Kao
Nianzhi Jiao
Yongyu Zhang
author_sort Zenghu Zhang
title Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
title_short Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
title_full Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
title_fullStr Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
title_full_unstemmed Long-Term Survival of <italic toggle="yes">Synechococcus</italic> and Heterotrophic Bacteria without External Nutrient Supply after Changes in Their Relationship from Antagonism to Mutualism
title_sort long-term survival of <italic toggle="yes">synechococcus</italic> and heterotrophic bacteria without external nutrient supply after changes in their relationship from antagonism to mutualism
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/4f13284c974441edae91de7af422fe4d
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