Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation

Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the legumin...

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Published ineLife Vol. 6
Main Authors Daubech, Benoit, Remigi, Philippe, Doin de Moura, Ginaini, Marchetti, Marta, Pouzet, Cécile, Auriac, Marie-Christine, Gokhale, Chaitanya S, Masson-Boivin, Catherine, Capela, Delphine
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 12.10.2017
eLife Sciences Publications Ltd
eLife Sciences Publication
eLife Sciences Publications, Ltd
Subjects
Agricultural ecology
Agricultural sciences
Analysis
Bacteria
Cupriavidus - growth & development
Cupriavidus - metabolism
Cupriavidus - physiology
Ecosystems
evolution
Evolutionary Biology
Fertilizers
Growth models
Infections
Inoculum
Legumes
Life Sciences
Medical research
Metabolism
Mimosa - microbiology
Mimosa - physiology
Mimosa pudica
Mutualism
Nitrogen
Nitrogen Fixation
Nodulation
Numerical analysis
Plant populations
Plants (Organisms)
Population
Proteins
Retirement benefits
rhizobium
Root nodules
Sanctions
Simulation
Soil microbiology
Spatio-Temporal Analysis
Sustainable agriculture
Symbionts
Symbiosis
Time
genomics
evolutionary biology
evolution
nitrogen fixation
rhizobium
symbiosis
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Abstract Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N )-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the system. N -fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N -fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N -fixation mutualistic trait.
AbstractList Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N )-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the system. N -fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N -fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N -fixation mutualistic trait.
Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N 2 )-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis–Mimosa pudica system. N 2 -fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N 2 -fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N 2 -fixation mutualistic trait. Rhizobia are soil bacteria that are able to form a symbiotic relationship with legumes – plants that include peas, beans and lentils. The bacteria move into cells in the roots of the plant and cause new organs called nodules to form. Inside the nodules the bacteria multiply before being released to the soil again. Also while in the nodules, the bacteria receive carbon-containing compounds from the plant. In return many of the bacteria convert (or “fix”) nitrogen from the air into compounds that the plant can use to build molecules such as DNA and proteins. Yet, some of the bacteria are “non-fixers” that provide little or no benefit to the host plant. Evidence suggests that legumes select against non-fixer bacteria, though it was not clear when or how this selection process occurs. Daubech, Remigi et al. have now followed the number and viability of two variants of a bacteria species called Cupriavidus taiwanensis as they form a symbiotic interaction with Mimosa pudica , a member of the pea family. The two types of bacteria differed only by whether or not they were able to fix nitrogen. At first fixers and non-fixers entered nodules and multiplied at equal rates. Later, the fixers progressively outcompeted the non-fixers. Then, around 20 days after the bacteria entered the plant, nodule cells that contained non-fixers degenerated. This indicates that the nodule cells help to control bacterial proliferation based on the benefits they receive in return. Further experiments and mathematical modeling also showed that over repeated cycles of root nodule formation, nitrogen fixers can invade a bacterial population dominated by non-fixer bacteria. The likelihood that this invasion will be successful increases as three other factors increase: the proportion of fixer bacteria in the initial population, the number of available plants, and the length of time the bacteria spend in the nodules. This mechanism ensures the maintenance and spread of nitrogen-fixing traits in the bacterial population. Improving the processes of biological nitrogen fixation could help to reduce the amount of fertilizers required to grow crops. This in the future could help make agricultural ecosystems more sustainable. The results presented by Daubech, Remigi et al. provide guidelines that could be used to select nitrogen-fixing bacteria on legume crops or on nitrogen-fixing cereals that may be engineered in the future. Further work is now needed to understand in more detail the molecular mechanisms that lead to the death of non-fixer bacteria.
Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis–Mimosa pudica system. N2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N2-fixation mutualistic trait.
Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis–Mimosa pudica system. N2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N2-fixation mutualistic trait. Rhizobia are soil bacteria that are able to form a symbiotic relationship with legumes – plants that include peas, beans and lentils. The bacteria move into cells in the roots of the plant and cause new organs called nodules to form. Inside the nodules the bacteria multiply before being released to the soil again. Also while in the nodules, the bacteria receive carbon-containing compounds from the plant. In return many of the bacteria convert (or “fix”) nitrogen from the air into compounds that the plant can use to build molecules such as DNA and proteins. Yet, some of the bacteria are “non-fixers” that provide little or no benefit to the host plant. Evidence suggests that legumes select against non-fixer bacteria, though it was not clear when or how this selection process occurs. Daubech, Remigi et al. have now followed the number and viability of two variants of a bacteria species called Cupriavidus taiwanensis as they form a symbiotic interaction with Mimosa pudica, a member of the pea family. The two types of bacteria differed only by whether or not they were able to fix nitrogen. At first fixers and non-fixers entered nodules and multiplied at equal rates. Later, the fixers progressively outcompeted the non-fixers. Then, around 20 days after the bacteria entered the plant, nodule cells that contained non-fixers degenerated. This indicates that the nodule cells help to control bacterial proliferation based on the benefits they receive in return. Further experiments and mathematical modeling also showed that over repeated cycles of root nodule formation, nitrogen fixers can invade a bacterial population dominated by non-fixer bacteria. The likelihood that this invasion will be successful increases as three other factors increase: the proportion of fixer bacteria in the initial population, the number of available plants, and the length of time the bacteria spend in the nodules. This mechanism ensures the maintenance and spread of nitrogen-fixing traits in the bacterial population. Improving the processes of biological nitrogen fixation could help to reduce the amount of fertilizers required to grow crops. This in the future could help make agricultural ecosystems more sustainable. The results presented by Daubech, Remigi et al. provide guidelines that could be used to select nitrogen-fixing bacteria on legume crops or on nitrogen-fixing cereals that may be engineered in the future. Further work is now needed to understand in more detail the molecular mechanisms that lead to the death of non-fixer bacteria.
Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N-2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis-Mimosa pudica system. N-2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N-2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N-2-fixation mutualistic trait.
Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N.sub.2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis--Mimosa pudica system. N.sub.2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N.sub.2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N.sub.2-fixation mutualistic trait.
Audience Academic
Author Auriac, Marie-Christine
Daubech, Benoit
Masson-Boivin, Catherine
Doin de Moura, Ginaini
Marchetti, Marta
Capela, Delphine
Pouzet, Cécile
Remigi, Philippe
Gokhale, Chaitanya S
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  organization: New Zealand Institute for Advanced Study, Massey University, Auckland, New Zealand
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  organization: The Laboratory of Plant-Microbe Interactions, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29022875$$D View this record in MEDLINE/PubMed
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Keywords genomics
evolutionary biology
evolution
nitrogen fixation
rhizobium
symbiosis
Language English
License Attribution: http://creativecommons.org/licenses/by
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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These authors contributed equally to this work.
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    fullname: Werner
SSID ssj0000748819
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Snippet Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a...
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SubjectTerms Agricultural ecology
Agricultural sciences
Analysis
Bacteria
Cupriavidus - growth & development
Cupriavidus - metabolism
Cupriavidus - physiology
Ecosystems
evolution
Evolutionary Biology
Fertilizers
Growth models
Infections
Inoculum
Legumes
Life Sciences
Medical research
Metabolism
Mimosa - microbiology
Mimosa - physiology
Mimosa pudica
Mutualism
Nitrogen
Nitrogen Fixation
Nodulation
Numerical analysis
Plant populations
Plants (Organisms)
Population
Proteins
Retirement benefits
rhizobium
Root nodules
Sanctions
Simulation
Soil microbiology
Spatio-Temporal Analysis
Sustainable agriculture
Symbionts
Symbiosis
Time
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Title Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation
URI https://www.ncbi.nlm.nih.gov/pubmed/29022875
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https://search.proquest.com/docview/1950417597
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https://pubmed.ncbi.nlm.nih.gov/PMC5687860
https://doaj.org/article/6050bb206c7e45199f3a2d054c2c2f15
Volume 6
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