Chemical signature of magnetotactic bacteria

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 6; pp. 1699 - 1703
• Main Authors: Amor, Matthieu, Busigny, Vincent, Durand-Dubief, Mickaël, Tharaud, Mickaël, Ona-Nguema, Georges, Gélabert, Alexandre, Alphandéry, Edouard, Menguy, Nicolas, Benedetti, Marc F., Chebbi, Imène, Guyot, François
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 10.02.2015; National Acad Sciences
• Subjects: Analysis of Variance; Bacteria; Biomarkers - analysis; Biomarkers - metabolism; Cell Culture Techniques; Fermentation; Ferrosoferric Oxide - chemical synthesis; Magnetite Nanoparticles - analysis; Magnetospirillum - chemistry; Magnetospirillum - growth & development; Magnetospirillum - metabolism; Magnetospirillum magneticum; Microscopy, Electron, Transmission; Mineralogy; Nanocrystals; Nanoparticles; Physical properties; Physical Sciences; Sciences of the Universe; Trace elements; Trace Elements - analysis; Trace Elements - metabolism; magnetite; magnetotactic bacteria; biomineralization; trace element incorporation
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1414112112

Significance Magnetite precipitates through either abiotic or biotic processes. Magnetotactic bacteria synthesize nanosized magnetite intracellularly and may represent one of the most ancient biomineralizing organisms. Thus, identifying bacterial magnetofossils in ancient sediments remains a key point to constrain life evolution over geological times. Although electron microscopy and magnetic characterizations allow identification of recent bacterial magnetofossils, sediment aging leads to variable dissolution or alteration of magnetite, potentially yielding crystals that barely preserve their structural integrity. Thus, reliable biosignatures surviving such modifications are still needed for distinguishing biogenic from abiotic magnetite. Here, we performed magnetotactic bacteria cultures and laboratory syntheses of abiotic magnetites. We quantified trace element incorporation into both types of magnetite, which allowed us to establish criteria for biomagnetite identification. There are longstanding and ongoing controversies about the abiotic or biological origin of nanocrystals of magnetite. On Earth, magnetotactic bacteria perform biomineralization of intracellular magnetite nanoparticles under a controlled pathway. These bacteria are ubiquitous in modern natural environments. However, their identification in ancient geological material remains challenging. Together with physical and mineralogical properties, the chemical composition of magnetite was proposed as a promising tracer for bacterial magnetofossil identification, but this had never been explored quantitatively and systematically for many trace elements. Here, we determine the incorporation of 34 trace elements in magnetite in both cases of abiotic aqueous precipitation and of production by the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1. We show that, in biomagnetite, most elements are at least 100 times less concentrated than in abiotic magnetite and we provide a quantitative pattern of this depletion. Furthermore, we propose a previously unidentified method based on strontium and calcium incorporation to identify magnetite produced by magnetotactic bacteria in the geological record.