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

Abstract

BackgroundMagnetotactic 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.ResultsGenomic 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 (Fe3O4) 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 materialThe online version of this article (doi:10.1186/s12864-016-3064-9) contains supplementary material, which is available to authorized users.

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

“…Third, crystal growth and morphology in strains WYHR‐1 (this study), AV‐1 (Lefèvre, Pósfai, et al, 2011), and MYR‐1 (Li et al, 2015) differ significantly from those in MTB of the Alphaproteobacteria and Gammaproteobacteria classes. Magnetotactic Alphaproteobacteria and Gammaproteobacteria generally biomineralize magnetite with symmetric morphologies, including octahedra ({111} forms) (Araujo et al, 2016; Zhang et al, 2017), cubo‐octahedra ({111} + {100} forms) (Faivre et al, 2008; Li, Ge, et al, 2013; Mann et al, 1984), and elongated hexagonal prisms ({111} + {110} + {100} forms) (Li et al, 2017; Meldrum et al, 1993a, 1993b). Unlike the multiple‐step growth for elongated asymmetric crystals observed in strains WYHR‐1 (this study), AV‐1 (Lefèvre, Pósfai, et al, 2011), and MYR‐1 (Li et al, 2015), symmetric crystals generally have homothetical growth, that is, constant width/length ratio in a given MTB species (Lefèvre, Trubitsyn, Abreu, Kolinko, Jogler, & de Almeida, 2013; Li et al, 2017; Meldrum et al, 1993a, 1993b; Sparks et al, 1990; Zhang et al, 2017).…”

“…Consistent with the phylogenetic and physiological diversity of MTB, magnetosomes also have diverse crystal morphologies and compositions (Pósfai, Lefèvre, et al, 2013). For instance, magnetotactic Alphaproteobacteria and Gammaproteobacteria biomineralize octahedral, cubo‐octahedral, or elongated‐prismatic crystals of magnetite, while MTB in the phyla Nitrospirae and Omnitrophica produce bullet‐shaped magnetite crystals (Araujo et al, 2016; Kolinko et al, 2016; Li, Ge, et al, 2013; Li et al, 2017; Meldrum et al, 1993a; Sparks et al, 1990; Zhang et al, 2017). Magnetotactic Deltaproteobacteria synthesize either magnetite‐type or greigite‐type crystals, or both within a single cell (Lefèvre & Bazylinski, 2013).…”

Biomineralization and Magnetism of Uncultured Magnetotactic Coccus Strain THC‐1 With Non‐chained Magnetosomal Magnetite Nanoparticles

“…Magnetotactic Deltaproteobacteria form bullet-shaped magnetite but with straight particles elongated along the [001] direction, with generally one flat {001} face (e.g., Candidatus Magnetcampylobacter weiyangensis strain WYHR-1) (Li, Menguy, et al, 2020) or a double triangle shape at its bottom (e.g., strains RS-1 and AV-1) Pósfai et al, 2006). In contrast, magnetotactic Alphaproteobacteria, Etaproteobacteria, and Gammaproteobacteria generally produce magnetite with symmetric morphologies, including octahedral {111} forms (e.g., Magnetofaba australis strain IT-1 and uncultured magnetotactic coccus strain SHHC-1) (Araujo et al, 2016;Zhang et al, 2017), cubo-octahedral ({111} + {100} forms) (e.g., Magnetotactic spirillum strains MS-1, MMS-1, MSR-1, and AMB-1) Li, Ge, et al, 2013;Mann et al, 1984;Meldrum et al, 1993a), and elongated hexagonal prisms with {111} + {110}…”

Biodiversity of Magnetotactic Bacteria in the Freshwater Lake Beloe Bordukovskoe, Russia

“…Although such magnetic enrichment approaches are efficient for isolation of environmental MTB, members of the Alphaproteobacteria and ‘Etaproteobacteria’ classes tend to predominate when these separation methods are used (14, 18–23). Since they are in higher concentration on the environment, are usually faster (24, 25) and more resistant to higher oxygen concentration than other MTB (26). The time used in standard concentration methods (20–30 minutes) make it hard the separation of MTB that have slow swimming ability (e.g., Magnetovibrio blakemorei MV-1) (27).…”