Chemical Signature of Magnetotactic Bacteria
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Chemical signature of magnetotactic bacteria Matthieu Amora,b,1, Vincent Busignya, Mickaël Durand-Dubiefc, Mickaël Tharauda, Georges Ona-Nguemab, Alexandre Gélaberta, Edouard Alphandéryb,c, Nicolas Menguyb, Marc F. Benedettia, Imène Chebbic, and François Guyotb aInstitut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, UMR 7154 CNRS, 75238 Paris, France; bInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Sorbonne Universités, Université Pierre et Marie Curie, UMR 7590 CNRS, Institut de Recherche pour le Développement UMR 206, Museum National d’Histoire Naturelle, 75252 Paris Cedex 05, France; and cNanobactérie SARL, 75016 Paris, France Edited by Mark H. Thiemens, University of California, San Diego, La Jolla, CA, and approved December 30, 2014 (received for review July 28, 2014) There are longstanding and ongoing controversies about the abiotic organic matter assembling magnetosomes (9, 14). This strongly or biological origin of nanocrystals of magnetite. On Earth, magne- complicates the identification of the bacterial magnetofossils. totactic bacteria perform biomineralization of intracellular magne- Moreover, those magnetites undergo variable transformations tite nanoparticles under a controlled pathway. These bacteria are ranging from isomorphic conversion to maghemite, all the way to ubiquitous in modern natural environments. However, their identi- crystals that just barely preserve the structural integrity (15). Thus, fication in ancient geological material remains challenging. Together for bacterial magnetofossil identification in ancient rock samples with physical and mineralogical properties, the chemical composi- reliable biosignatures surviving these modifications are still needed tion of magnetite was proposed as a promising tracer for bacterial for distinguishing biogenic from abiotic magnetite (1, 2). magnetofossil identification, but this had never been explored Geochemical fingerprints can be used as a potential tool for quantitatively and systematically for many trace elements. Here, identifying fossilized biominerals (2, 16). For instance, chemical we determine the incorporation of 34 trace elements in magnetite purity has been suggested as a common feature of minerals in both cases of abiotic aqueous precipitation and of production by produced by living organisms (2). The chemical purity of mag- the magnetotactic bacterium Magnetospirillum magneticum strain netite from MTB has been discussed for many years (e.g., ref. AMB-1. We show that, in biomagnetite, most elements are at least 17). Although not without controversy, it was suggested that low 100 times less concentrated than in abiotic magnetite and we concentrations in minor elements observed in magnetite from provide a quantitative pattern of this depletion. Furthermore, Martian meteorite ALH84001 could indicate a biological origin we propose a previously unidentified method based on strontium for magnetite (18). This interpretation was supported by abiotic and calcium incorporation to identify magnetite produced by formation of magnetite in the laboratory, leading to high levels magnetotactic bacteria in the geological record. of elements other than iron in the crystal products (19, 20), ex- cept if initial materials highly depleted in doping elements were magnetotactic bacteria | magnetite | biomineralization | used (21). However, the degree of magnetite chemical purity in trace element incorporation these previous studies was estimated by energy dispersive x-ray spectroscopy (EDXS) coupled with transmission electron mi- agnetite (Fe3O4) is a widespread iron oxide found in geo- croscopy, which is usually limited to the quantification of rela- Mlogical sedimentary deposits such as banded iron formations, tively elevated elemental concentrations, typically higher than carbonate platforms, or paleosols (1). It can be produced through 0.1–1% (22). Moreover, EDXS analyses have been used to abiotic or biotic pathways. Magnetotactic bacteria (MTB) and evaluate single-element incorporations into magnetite crystals dissimilatory iron-reducing bacteria are known to synthetize produced by MTB (23–26). These experiments tested only high magnetite nanoparticles (2). MTB are magnetite- or greigite (Fe3S4)-producing bacteria Significance found in both freshwater and marine environments. They inhabit the oxic–anoxic transition zone under microaerophilic conditions Magnetite precipitates through either abiotic or biotic pro- required for their growth. Magnetite or greigite crystals are ac- EARTH, ATMOSPHERIC, cesses. Magnetotactic bacteria synthesize nanosized magnetite AND PLANETARY SCIENCES tively precipitated through biological mechanisms in intracellular intracellularly and may represent one of the most ancient organelles called magnetosomes (e.g., refs. 3 and 4). Magneto- biomineralizing organisms. Thus, identifying bacterial magne- somes are assembled in chains inside the cell (Fig. 1) and provide tofossils in ancient sediments remains a key point to constrain the microorganism with a permanent magnetic dipole. This ar- life evolution over geological times. Although electron mi- rangement allows the bacteria to align themselves along the croscopy and magnetic characterizations allow identification of Earth’s geomagnetic field and to reach the optimal position along recent bacterial magnetofossils, sediment aging leads to vari- vertical chemical gradients (5, 6). When the cell dies, magneto- able dissolution or alteration of magnetite, potentially yielding somes may be deposited and trapped into sediments. Magnetite crystals that barely preserve their structural integrity. Thus, can then be fossilized if the redox conditions are appropriate (1). reliable biosignatures surviving such modifications are still This mineral may thus be an indirect bacterial fossil. Magneto- needed for distinguishing biogenic from abiotic magnetite. tactic bacteria have been proposed to represent one of the most Here, we performed magnetotactic bacteria cultures and lab- ancient biomineralizing organisms (1, 7). Thus, the identification oratory syntheses of abiotic magnetites. We quantified trace of fossil magnetotactic bacteria, hereafter named bacterial mag- element incorporation into both types of magnetite, which netofossils, would provide strong constraints on the evolution of allowed us to establish criteria for biomagnetite identification. life and of biomineralization over geological times. Magnetite produced by MTB shows highly controlled crystal- Author contributions: V.B. and F.G. designed research; M.A. and N.M. performed re- lographic structure (8). It displays narrow size distributions and is search; M.D.-D., M.T., G.O.-N., A.G., E.A., N.M., M.F.B., and I.C. contributed new in the magnetic stable single-domain range. Magnetosome chains reagents/analytic tools; M.A., V.B., G.O.-N., A.G., and F.G. analyzed data; and M.A., V.B., have remarkable magnetic properties (5, 6, 9), which have been and F.G. wrote the paper. used to identify bacterial magnetofossils in sediments. Although The authors declare no conflict of interest. previous studies demonstrated that observations by electron mi- This article is a PNAS Direct Submission. croscopy and/or magnetic measurements could detect bacterial 1To whom correspondence should be addressed. Email: [email protected]. – magnetofossils in natural samples (9 13), the chain structure is This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. generally lost during sediment aging owing to degradation of 1073/pnas.1414112112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1414112112 PNAS | February 10, 2015 | vol. 112 | no. 6 | 1699–1703 Downloaded by guest on September 28, 2021 (ii) in bottles following ATCC recommendations. The initial growth media of the two experiments were different. In contrast with bottle cultures, pH and pO2 were maintained constant in the fermentor and the medium was continuously homogenized by stirring. These contrasting conditions allow us to evaluate the variability possibly induced by the biosynthesis. In either case, the bacterial growth medium was doped with the same 34 trace ele- ments at 100 ppb each, (i.e., at the same doping level as in the abiotic syntheses). Chains of magnetosomes were extracted from cells with a high-pressure homogenizer. Magnetosome membranes surrounding magnetite were removed using a Triton-SDS-phenol solution heated at 70 °C overnight. Magnetite nanoparticles were leached with ultrapure water and contaminant-free EDTA solu- tion to chelate and remove any element adsorbed on mineral surface (Fig. 1). Abiotic and biotic bottle experiments were carried out in duplicate. Mineralogical characterization (i.e., size, shape, and structure) of the magnetite samples was obtained from X-ray diffraction and transmission electron microscopy (Fig. 1 and Fig. S1). The element concentrations in all experimental products were measured by high-resolution inductively coupled plasma mass spectrometry. Results and Discussion Partition Coefficients Between Magnetite and Aqueous Solution. For both biotic and abiotic experiments, elemental partitioning be- tween magnetite and solution is described herein by the partition coefficient normalized to iron: Ci Ci Ki;Fe = Mag Sol; [1] Fe Fe CMag CSol where i is the element under consideration and CMag and CSol are the concentrations in magnetite and residual solution after pre- cipitation, respectively. Partition coefficients are more relevant Fig. 1. Transmission electron