<i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway

Inter-organismal metabolites play important roles in regulating organism behavior and the communication between organisms. Nematodes, the most abundant animals on earth, are crucial participants in soil ecosystems through their interactions with microbes. For example, bacterial-feeding nematodes inc...

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Main Authors: Mengsha Li, Teng Li, Ming Zhou, Mengdi Li, Yexin Zhao, Jingjing Xu, Feng Hu, Huixin Li
Format: Article
Language:English
Published: MDPI AG 2021-04-01
Series:Microorganisms
Subjects:
IAA
Online Access:https://www.mdpi.com/2076-2607/9/5/970
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spelling doaj-a0ac8f0dbfc9403f89d6dac312e2bd1c2021-04-30T23:00:58ZengMDPI AGMicroorganisms2076-26072021-04-01997097010.3390/microorganisms9050970<i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid PathwayMengsha Li0Teng Li1Ming Zhou2Mengdi Li3Yexin Zhao4Jingjing Xu5Feng Hu6Huixin Li7College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaInter-organismal metabolites play important roles in regulating organism behavior and the communication between organisms. Nematodes, the most abundant animals on earth, are crucial participants in soil ecosystems through their interactions with microbes. For example, bacterial-feeding nematodes increase the activity of indole-3-acetic acid (IAA)-producing bacteria and the IAA content in soil. However, the way in which these nematodes interact with bacteria and affect IAA biosynthesis is not well understood. Here, using the model nematode <i>Caenorhabditis elegans</i> and the plant-beneficial bacterium <i>Arthrobacter pascens</i> ZZ21, we examined the effects of nematode excretions or extracts on bacterial IAA biosynthesis. To explore the underlying regulatory mechanism in more detail, we performed transcriptome sequencing and metabolomic analysis. Our findings suggest that <i>C. elegans</i> extracts promote IAA biosynthesis in <i>A. pascens</i> ZZ21 by increasing the expression of genes and the abundance of intermediates involved in the indole-3-pyruvic acid (IPyA) pathway. <i>C. elegans</i> extracts also significantly influenced biosynthetic and metabolic activity in <i>A. pascens</i> ZZ21. Treatment with <i>C. elegans</i> extracts promoted pyruvate metabolism, the citrate cycle (TCA) cycle and the production of some TCA-cycle-related amino acids and inhibited oxidative phosphorylation, which induced the accumulation of reduced nicotinamide adenine dinucleotide (NADH). We propose that the extracts altered the metabolism of <i>A. pascens</i> ZZ21 to help the bacteria resist stress caused by their predator. Our findings indicate that bacterial-feeding nematodes mediate the interaction between nematodes and bacteria via their extracts, providing insights into the ecological function of <i>C. elegans</i> in soil.https://www.mdpi.com/2076-2607/9/5/970<i>C. elegans</i> extractsIAA-producing bacteriaIAAindole-3-pyruvic acid pathwaypyruvateNADH
collection DOAJ
language English
format Article
sources DOAJ
author Mengsha Li
Teng Li
Ming Zhou
Mengdi Li
Yexin Zhao
Jingjing Xu
Feng Hu
Huixin Li
spellingShingle Mengsha Li
Teng Li
Ming Zhou
Mengdi Li
Yexin Zhao
Jingjing Xu
Feng Hu
Huixin Li
<i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
Microorganisms
<i>C. elegans</i> extracts
IAA-producing bacteria
IAA
indole-3-pyruvic acid pathway
pyruvate
NADH
author_facet Mengsha Li
Teng Li
Ming Zhou
Mengdi Li
Yexin Zhao
Jingjing Xu
Feng Hu
Huixin Li
author_sort Mengsha Li
title <i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
title_short <i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
title_full <i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
title_fullStr <i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
title_full_unstemmed <i>Caenorhabditis elegans</i> Extracts Stimulate IAA Biosynthesis in <i>Arthrobacter pascens</i> ZZ21 via the Indole-3-pyruvic Acid Pathway
title_sort <i>caenorhabditis elegans</i> extracts stimulate iaa biosynthesis in <i>arthrobacter pascens</i> zz21 via the indole-3-pyruvic acid pathway
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2021-04-01
description Inter-organismal metabolites play important roles in regulating organism behavior and the communication between organisms. Nematodes, the most abundant animals on earth, are crucial participants in soil ecosystems through their interactions with microbes. For example, bacterial-feeding nematodes increase the activity of indole-3-acetic acid (IAA)-producing bacteria and the IAA content in soil. However, the way in which these nematodes interact with bacteria and affect IAA biosynthesis is not well understood. Here, using the model nematode <i>Caenorhabditis elegans</i> and the plant-beneficial bacterium <i>Arthrobacter pascens</i> ZZ21, we examined the effects of nematode excretions or extracts on bacterial IAA biosynthesis. To explore the underlying regulatory mechanism in more detail, we performed transcriptome sequencing and metabolomic analysis. Our findings suggest that <i>C. elegans</i> extracts promote IAA biosynthesis in <i>A. pascens</i> ZZ21 by increasing the expression of genes and the abundance of intermediates involved in the indole-3-pyruvic acid (IPyA) pathway. <i>C. elegans</i> extracts also significantly influenced biosynthetic and metabolic activity in <i>A. pascens</i> ZZ21. Treatment with <i>C. elegans</i> extracts promoted pyruvate metabolism, the citrate cycle (TCA) cycle and the production of some TCA-cycle-related amino acids and inhibited oxidative phosphorylation, which induced the accumulation of reduced nicotinamide adenine dinucleotide (NADH). We propose that the extracts altered the metabolism of <i>A. pascens</i> ZZ21 to help the bacteria resist stress caused by their predator. Our findings indicate that bacterial-feeding nematodes mediate the interaction between nematodes and bacteria via their extracts, providing insights into the ecological function of <i>C. elegans</i> in soil.
topic <i>C. elegans</i> extracts
IAA-producing bacteria
IAA
indole-3-pyruvic acid pathway
pyruvate
NADH
url https://www.mdpi.com/2076-2607/9/5/970
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