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Inherent tendency of Synechococcus and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference.

ABSTRACT: Mutualism between Synechococcus and heterotrophic bacteria has been found to support their prolonged survival in nutrient-depleted conditions. However, environmental interference on the fate of their mutualism is not understood. Here, we show that exogenous nutrients disrupt their established mutualism. Once the exogenous nutrients were exhausted, Synechococcus and heterotrophic bacteria gradually reestablished their metabolic mutualism during 450 days of culture, which revived unhealthy Synechococcus cells. Using metagenomics, metatranscriptomics, and the ¹⁵N tracer method, we reveal that the associated bacterial nitrogen fixation triggered the reestablishment of the mutualism and revival of Synechococcus health. During this process, bacterial community structure and functions underwent tremendous adjustments to achieve the driving effect, and a cogeneration of nitrogen, phosphorus, iron, and vitamin by the heterotrophic bacteria sustained Synechococcus's prolonged healthy growth. Our findings suggest that Synechococcus and heterotrophic bacteria may have an inherent tendency toward mutualism despite environmental interference. This may exhibit their coevolutionary adaptations in nutrient-deficient environments.

SUBMITTER: Nair S

PROVIDER: S-EPMC9524826 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Inherent tendency of Synechococcus and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference.

Nair Shailesh S Zhang Zenghu Z Li Hongmei H Zhao Hanshuang H Shen Hui H Kao Shuh-Ji SJ Jiao Nianzhi N Zhang Yongyu Y

Science advances 20220930 39

Mutualism between Synechococcus and heterotrophic bacteria has been found to support their prolonged survival in nutrient-depleted conditions. However, environmental interference on the fate of their mutualism is not understood. Here, we show that exogenous nutrients disrupt their established mutualism. Once the exogenous nutrients were exhausted, Synechococcus and heterotrophic bacteria gradually reestablished their metabolic mutualism during 450 days of culture, which revived unh ...[more]

PMID: 36179022

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Project description: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.

Project description:Interactions between photoautotrophic and heterotrophic microorganisms are central to the marine microbial ecosystem. Lab cultures of one of the dominant marine photoautotrophs, Synechococcus, have historically been difficult to render axenic, presumably because these bacteria depend upon other organisms to grow under these conditions. These tight associations between Synechococcus and heterotrophic bacteria represent a good relevant system to study interspecies interactions. Ten individual Synechococcus strains, isolated from eutrophic and oligotrophic waters, were chosen for investigation. Four to six dominant associated heterotrophic bacteria were detected in the liquid cultures of each Synechococcus isolate, comprising members of the Cytophaga-Flavobacteria-Bacteroides (CFB) group (mainly from Flavobacteriales and Cytophagales), Alphaproteobacteria (mainly from the Roseobacter clade), Gammaproteobacteria (mainly from the Alteromonadales and Pseudomonadales), and Actinobacteria The presence of the CFB group, Gammaproteobacteria, and Actinobacteria showed clear geographic patterns related to the isolation environments of the Synechococcus bacteria. An investigation of the population dynamics within a growing culture (XM-24) of one of the isolates, including an evaluation of the proportions of cells that were free-living versus aggregated/attached, revealed interesting patterns for different bacterial groups. In Synechococcus sp. strain XM-24 culture, flavobacteria, which was the most abundant group throughout the culture period, tended to be aggregated or attached to the Synechococcus cells, whereas the actinobacteria demonstrated a free-living lifestyle, and roseobacters displayed different patterns depending on the culture growth phase. Factors contributing to these succession patterns for the heterotrophs likely include interactions among the culture community members, their relative abilities to utilize different compounds produced by Synechococcus cells and changes in the compounds released as culture growth proceeds, and their responses to other changes in the environmental conditions throughout the culture period.IMPORTANCE Marine microbes exist within an interactive ecological network, and studying their interactions is an important part of understanding their roles in global biogeochemical cycling and the determinants of microbial diversity. In this study, the dynamic relationships between Synechococcus spp. and their associated heterotrophic bacteria were investigated. Synechococcus-associated heterotrophic bacteria had similar geographic distribution patterns as their "host" and displayed different lifestyles (free-living versus attached/aggregated) according to the Synechococcus culture growth phases. Combined organic carbon composition and bacterial lifestyle data indicated a potential for succession in carbon utilization patterns by the dominant associated heterotrophic bacteria. Comprehending the interactions between photoautotrophs and heterotrophs and the patterns of organic carbon excretion and utilization is critical to understanding their roles in oceanic biogeochemical cycling.

Dataset Information

Inherent tendency of Synechococcus and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference.

Publications

Inherent tendency of <i>Synechococcus</i> and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference.

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