Dataset Information

Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth.

ABSTRACT: The proficiency of phyllosphere microbiomes in efficiently utilizing plant-provided nutrients is pivotal for their successful colonization of plants. The methylotrophic capabilities of Methylobacterium/Methylorubrum play a crucial role in this process. However, the precise mechanisms facilitating efficient colonization remain elusive. In the present study, we investigate the significance of methanol assimilation in shaping the success of mutualistic relationships between methylotrophs and plants. A set of strains originating from Methylorubrum extorquens AM1 are subjected to evolutionary pressures to thrive under low methanol conditions. A mutation in the phosphoribosylpyrophosphate synthetase gene is identified, which converts it into a metabolic valve. This valve redirects limited C1-carbon resources towards the synthesis of biomass by up-regulating a non-essential phosphoketolase pathway. These newly acquired bacterial traits demonstrate superior colonization capabilities, even at low abundance, leading to increased growth of inoculated plants. This function is prevalent in Methylobacterium/Methylorubrum strains. In summary, our findings offer insights that could guide the selection of Methylobacterium/Methylorubrum strains for advantageous agricultural applications.

SUBMITTER: Zhang C

PROVIDER: S-EPMC11252147 | biostudies-literature | 2024 Jul

REPOSITORIES: biostudies-literature

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Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth.

Zhang Cong C Zhou Di-Fei DF Wang Meng-Ying MY Song Ya-Zhen YZ Zhang Chong C Zhang Ming-Ming MM Sun Jing J Yao Lu L Mo Xu-Hua XH Ma Zeng-Xin ZX Yuan Xiao-Jie XJ Shao Yi Y Wang Hao-Ran HR Dong Si-Han SH Bao Kai K Lu Shu-Huan SH Sadilek Martin M Kalyuzhnaya Marina G MG Xing Xin-Hui XH Yang Song S

Nature communications 20240716 1

The proficiency of phyllosphere microbiomes in efficiently utilizing plant-provided nutrients is pivotal for their successful colonization of plants. The methylotrophic capabilities of Methylobacterium/Methylorubrum play a crucial role in this process. However, the precise mechanisms facilitating efficient colonization remain elusive. In the present study, we investigate the significance of methanol assimilation in shaping the success of mutualistic relationships between methylotrophs and plants ...[more]

PMID: 39013920

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Project description:The genus Methylobacterium includes widespread plant-associated bacteria that are abundant in the plant phyllosphere (leaf surfaces), consume plant-secreted methanol, and can produce plant growth-promoting metabolites. However, despite the potential to increase agricultural productivity, their impact on host fitness in the natural environment is relatively poorly understood. Here, we conducted field experiments with three traditionally cultivated rice landraces from northeastern India. We inoculated seedlings with native versus nonnative phyllosphere Methylobacterium strains and found significant impacts on plant growth and grain yield. However, these effects were variable. Whereas some Methylobacterium isolates were beneficial for their host, others had no impact or were no more beneficial than the bacterial growth medium on its own. Host plant benefits were not consistently associated with Methylobacterium colonization and did not have altered phyllosphere microbiome composition, changes in the early expression of plant stress response pathways, or bacterial auxin production. We provide the first demonstration of the benefits of phyllosphere Methylobacterium for rice yield under field conditions and highlight the need for further analysis to understand the mechanisms underlying these benefits. Given that the host landrace-Methylobacterium relationship was not generalizable, future agricultural applications will require careful testing to identify coevolved host-bacterium pairs that may enhance the productivity of high-value rice varieties. IMPORTANCE Plants are associated with diverse microbes in nature. Do the microbes increase host plant health, and can they be used for agricultural applications? This is an important question that must be answered in the field rather than in the laboratory or greenhouse. We tested the effects of native, leaf-inhabiting bacteria (genus Methylobacterium) on traditionally cultivated rice varieties in a crop field. We found that inoculation with some bacteria increased rice grain production substantially while a nonnative bacterium reduced plant health. Overall, the effect of bacterial inoculation varied across pairs of rice varieties and their native bacteria. Thus, knowledge of evolved associations between specific bacteria hosted by specific rice varieties is necessary to develop ways to increase the yield of traditional rice landraces and preserve these important sources of cultural and genetic diversity.

Project description:Motile bacteria take a competitive advantage in colonization of plant surfaces to establish beneficial associations that eventually support plant health. Plant exudates serve not only as primary growth substrates for bacteria but also as bacterial chemotaxis attractants. A number of plant-derived compounds and corresponding chemotaxis sensors have been documented, however, the sensors for methanol, one of the major volatile compounds released by plants, have not been identified. Methylobacterium species are ubiquitous plant surface-symbiotic, methylotrophic bacteria. A plant-growth promoting bacterium, M. aquaticum strain 22A exhibits chemotaxis toward methanol (methylotaxis). Its genome encodes 52 methyl-accepting chemotaxis proteins (MCPs), among which we identified three MCPs (methylotaxis proteins, MtpA, MtpB, and MtpC) responsible for methylotaxis. The triple gene mutant of the MCPs exhibited no methylotaxis, slower gathering to plant tissues, and less efficient colonization on plants than the wild type, suggesting that the methylotaxis mediates initiation of plant-Methylobacterium symbiosis and engages in proliferation on plants. To examine how these MCPs are operating methylotaxis, we generated multiple gene knockouts of the MCPs, and Ca2+-dependent MxaFI and lanthanide (Ln3+)-dependent XoxF methanol dehydrogenases (MDHs), whose expression is regulated by the presence of Ln3+. MtpA was found to be a cytosolic sensor that conducts formaldehyde taxis (formtaxis), as well as methylotaxis when MDHs generate formaldehyde. MtpB contained a dCache domain and exhibited differential cellular localization in response to La3+. MtpB expression was induced by La3+, and its activity required XoxF1. MtpC exhibited typical cell pole localization, required MxaFI activity, and was regulated under MxbDM that is also required for MxaF expression. Strain 22A methylotaxis is realized by three independent MCPs, two of which monitor methanol oxidation by Ln3+-regulated MDHs, and one of which monitors the common methanol oxidation product, formaldehyde. We propose that methanol metabolism-linked chemotaxis is the key factor for the efficient colonization of Methylobacterium on plants.

Dataset Information

Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth.

Publications

Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth.

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