Bacterial community function increases leaf growth in a pitcher plant experimental system

ABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant g...

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Main Authors: Jessica R. Bernardin, Erica B. Young, Sarah M. Gray, Leonora S. Bittleston
Format: Article
Language:English
Published: American Society for Microbiology 2024-12-01
Series:mSystems
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Online Access:https://journals.asm.org/doi/10.1128/msystems.01298-24
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author Jessica R. Bernardin
Erica B. Young
Sarah M. Gray
Leonora S. Bittleston
author_facet Jessica R. Bernardin
Erica B. Young
Sarah M. Gray
Leonora S. Bittleston
author_sort Jessica R. Bernardin
collection DOAJ
description ABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community’s functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, including S. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth.IMPORTANCEThis study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions.
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spelling doaj-art-ede4a91efcd84f55b53205c50f9237f42024-12-17T14:21:13ZengAmerican Society for MicrobiologymSystems2379-50772024-12-0191210.1128/msystems.01298-24Bacterial community function increases leaf growth in a pitcher plant experimental systemJessica R. Bernardin0Erica B. Young1Sarah M. Gray2Leonora S. Bittleston3Department of Biological Sciences, Boise State University, Boise, Idaho, USADepartment of Biological Sciences and School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin, USADepartment of Biology-Ecology and Evolution, University of Fribourg, Fribourg, SwitzerlandDepartment of Biological Sciences, Boise State University, Boise, Idaho, USAABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community’s functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, including S. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth.IMPORTANCEThis study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions.https://journals.asm.org/doi/10.1128/msystems.01298-24microbial community functionmetatranscriptomicsphyllospheremicrobe-plant interactionshost healthmetagenomics
spellingShingle Jessica R. Bernardin
Erica B. Young
Sarah M. Gray
Leonora S. Bittleston
Bacterial community function increases leaf growth in a pitcher plant experimental system
mSystems
microbial community function
metatranscriptomics
phyllosphere
microbe-plant interactions
host health
metagenomics
title Bacterial community function increases leaf growth in a pitcher plant experimental system
title_full Bacterial community function increases leaf growth in a pitcher plant experimental system
title_fullStr Bacterial community function increases leaf growth in a pitcher plant experimental system
title_full_unstemmed Bacterial community function increases leaf growth in a pitcher plant experimental system
title_short Bacterial community function increases leaf growth in a pitcher plant experimental system
title_sort bacterial community function increases leaf growth in a pitcher plant experimental system
topic microbial community function
metatranscriptomics
phyllosphere
microbe-plant interactions
host health
metagenomics
url https://journals.asm.org/doi/10.1128/msystems.01298-24
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