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Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment

BACKGROUND: Magnetotactic bacteria (MTB) are a unique group of prokaryotes that have a potentially high impact on global geochemical cycling of significant primary elements because of their metabolic plasticity and the ability to biomineralize iron-rich magnetic particles called magnetosomes. Unders...

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Autores principales: Araujo, Ana Carolina Vieira, Morillo, Viviana, Cypriano, Jefferson, Teixeira, Lia Cardoso Rocha Saraiva, Leão, Pedro, Lyra, Sidcley, Almeida, Luiz Gonzaga de, Bazylinski, Dennis A., Vasconcellos, Ana Tereza Ribeiro de, Abreu, Fernanda, Lins, Ulysses
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5088516/
https://www.ncbi.nlm.nih.gov/pubmed/27801294
http://dx.doi.org/10.1186/s12864-016-3064-9
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author Araujo, Ana Carolina Vieira
Morillo, Viviana
Cypriano, Jefferson
Teixeira, Lia Cardoso Rocha Saraiva
Leão, Pedro
Lyra, Sidcley
Almeida, Luiz Gonzaga de
Bazylinski, Dennis A.
Vasconcellos, Ana Tereza Ribeiro de
Abreu, Fernanda
Lins, Ulysses
author_facet Araujo, Ana Carolina Vieira
Morillo, Viviana
Cypriano, Jefferson
Teixeira, Lia Cardoso Rocha Saraiva
Leão, Pedro
Lyra, Sidcley
Almeida, Luiz Gonzaga de
Bazylinski, Dennis A.
Vasconcellos, Ana Tereza Ribeiro de
Abreu, Fernanda
Lins, Ulysses
author_sort Araujo, Ana Carolina Vieira
collection PubMed
description BACKGROUND: Magnetotactic bacteria (MTB) are a unique group of prokaryotes that have a potentially high impact on global geochemical cycling of significant primary elements because of their metabolic plasticity and the ability to biomineralize iron-rich magnetic particles called magnetosomes. Understanding the genetic composition of the few cultivated MTB along with the unique morphological features of this group of bacteria may provide an important framework for discerning their potential biogeochemical roles in natural environments. RESULTS: Genomic and ultrastructural analyses were combined to characterize the cultivated magnetotactic coccus Magnetofaba australis strain IT-1. Cells of this species synthesize a single chain of elongated, cuboctahedral magnetite (Fe(3)O(4)) magnetosomes that cause them to align along magnetic field lines while they swim being propelled by two bundles of flagella at velocities up to 300 μm s(−1). High-speed microscopy imaging showed the cells move in a straight line rather than in the helical trajectory described for other magnetotactic cocci. Specific genes within the genome of Mf. australis strain IT-1 suggest the strain is capable of nitrogen fixation, sulfur reduction and oxidation, synthesis of intracellular polyphosphate granules and transporting iron with low and high affinity. Mf. australis strain IT-1 and Magnetococcus marinus strain MC-1 are closely related phylogenetically although similarity values between their homologous proteins are not very high. CONCLUSION: Mf. australis strain IT-1 inhabits a constantly changing environment and its complete genome sequence reveals a great metabolic plasticity to deal with these changes. Aside from its chemoautotrophic and chemoheterotrophic metabolism, genomic data indicate the cells are capable of nitrogen fixation, possess high and low affinity iron transporters, and might be capable of reducing and oxidizing a number of sulfur compounds. The relatively large number of genes encoding transporters as well as chemotaxis receptors in the genome of Mf. australis strain IT-1 combined with its rapid swimming velocities, indicate that cells respond rapidly to environmental changes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3064-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-50885162016-11-07 Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment Araujo, Ana Carolina Vieira Morillo, Viviana Cypriano, Jefferson Teixeira, Lia Cardoso Rocha Saraiva Leão, Pedro Lyra, Sidcley Almeida, Luiz Gonzaga de Bazylinski, Dennis A. Vasconcellos, Ana Tereza Ribeiro de Abreu, Fernanda Lins, Ulysses BMC Genomics Research BACKGROUND: Magnetotactic bacteria (MTB) are a unique group of prokaryotes that have a potentially high impact on global geochemical cycling of significant primary elements because of their metabolic plasticity and the ability to biomineralize iron-rich magnetic particles called magnetosomes. Understanding the genetic composition of the few cultivated MTB along with the unique morphological features of this group of bacteria may provide an important framework for discerning their potential biogeochemical roles in natural environments. RESULTS: Genomic and ultrastructural analyses were combined to characterize the cultivated magnetotactic coccus Magnetofaba australis strain IT-1. Cells of this species synthesize a single chain of elongated, cuboctahedral magnetite (Fe(3)O(4)) magnetosomes that cause them to align along magnetic field lines while they swim being propelled by two bundles of flagella at velocities up to 300 μm s(−1). High-speed microscopy imaging showed the cells move in a straight line rather than in the helical trajectory described for other magnetotactic cocci. Specific genes within the genome of Mf. australis strain IT-1 suggest the strain is capable of nitrogen fixation, sulfur reduction and oxidation, synthesis of intracellular polyphosphate granules and transporting iron with low and high affinity. Mf. australis strain IT-1 and Magnetococcus marinus strain MC-1 are closely related phylogenetically although similarity values between their homologous proteins are not very high. CONCLUSION: Mf. australis strain IT-1 inhabits a constantly changing environment and its complete genome sequence reveals a great metabolic plasticity to deal with these changes. Aside from its chemoautotrophic and chemoheterotrophic metabolism, genomic data indicate the cells are capable of nitrogen fixation, possess high and low affinity iron transporters, and might be capable of reducing and oxidizing a number of sulfur compounds. The relatively large number of genes encoding transporters as well as chemotaxis receptors in the genome of Mf. australis strain IT-1 combined with its rapid swimming velocities, indicate that cells respond rapidly to environmental changes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3064-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-10-25 /pmc/articles/PMC5088516/ /pubmed/27801294 http://dx.doi.org/10.1186/s12864-016-3064-9 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Araujo, Ana Carolina Vieira
Morillo, Viviana
Cypriano, Jefferson
Teixeira, Lia Cardoso Rocha Saraiva
Leão, Pedro
Lyra, Sidcley
Almeida, Luiz Gonzaga de
Bazylinski, Dennis A.
Vasconcellos, Ana Tereza Ribeiro de
Abreu, Fernanda
Lins, Ulysses
Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title_full Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title_fullStr Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title_full_unstemmed Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title_short Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
title_sort combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5088516/
https://www.ncbi.nlm.nih.gov/pubmed/27801294
http://dx.doi.org/10.1186/s12864-016-3064-9
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