Modeling aerotaxis band formation in Azospirillum brasilense

Abstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense...

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Main Authors: Mustafa Elmas, Vasilios Alexiades, Lindsey O’Neal, Gladys Alexandre
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-019-1468-9
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spelling doaj-285b53baef1c4d31a757bd59b09d5c542020-11-25T02:26:53ZengBMCBMC Microbiology1471-21802019-05-0119111010.1186/s12866-019-1468-9Modeling aerotaxis band formation in Azospirillum brasilenseMustafa Elmas0Vasilios Alexiades1Lindsey O’Neal2Gladys Alexandre3Mathematics, University of TennesseeMathematics, University of TennesseeBiochemistry and Cellular & Molecular Biology, University of TennesseeBiochemistry and Cellular & Molecular Biology, University of TennesseeAbstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.http://link.springer.com/article/10.1186/s12866-019-1468-9ChemotaxisAerotaxisBand formationAzospirillum brasilenseMathematical modeling
collection DOAJ
language English
format Article
sources DOAJ
author Mustafa Elmas
Vasilios Alexiades
Lindsey O’Neal
Gladys Alexandre
spellingShingle Mustafa Elmas
Vasilios Alexiades
Lindsey O’Neal
Gladys Alexandre
Modeling aerotaxis band formation in Azospirillum brasilense
BMC Microbiology
Chemotaxis
Aerotaxis
Band formation
Azospirillum brasilense
Mathematical modeling
author_facet Mustafa Elmas
Vasilios Alexiades
Lindsey O’Neal
Gladys Alexandre
author_sort Mustafa Elmas
title Modeling aerotaxis band formation in Azospirillum brasilense
title_short Modeling aerotaxis band formation in Azospirillum brasilense
title_full Modeling aerotaxis band formation in Azospirillum brasilense
title_fullStr Modeling aerotaxis band formation in Azospirillum brasilense
title_full_unstemmed Modeling aerotaxis band formation in Azospirillum brasilense
title_sort modeling aerotaxis band formation in azospirillum brasilense
publisher BMC
series BMC Microbiology
issn 1471-2180
publishDate 2019-05-01
description Abstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
topic Chemotaxis
Aerotaxis
Band formation
Azospirillum brasilense
Mathematical modeling
url http://link.springer.com/article/10.1186/s12866-019-1468-9
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