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Putative greigite magnetofossils from thePliocene epoch
IULIANA VASILIEV1*, CHRISTINE FRANKE1†, JOHANNES D. MEELDIJK2, MARK J. DEKKERS1,COR G. LANGEREIS1 AND WOUT KRIJGSMAN1
1Paleomagnetic Laboratory ‘Fort Hoofddijk’, Department of Earth Sciences, Utrecht University, Budapestlaan 17, 3584 CD, Utrecht, The Netherlands2Department of Chemistry, Utrecht University, Sorbonnelaan 16, 3545 CA Utrecht, The Netherlands†Current address: Laboratoire des Sciences du Climat et de l’Environnement, CEA-CNRS-UVSQ, Campus du CNRS, Bat. 12, Avenue de la Terrasse, 91198 Gif-sur-YvetteCedex, France*e-mail: [email protected]
Published online: 19 October 2008; doi:10.1038/ngeo335
Magnetotactic bacteria produce chains of magnetite1,2 and/orgreigite3–5 crystals within their cell bodies called magnetosomesthat are permanently magnetized6. They use these magnetsto navigate along geomagnetic field lines to reach theirpreferred habitat7. Greigite magnetosomes have been welldocumented in modern sedimentary environments, but theiridentification in the fossil record remains controversial. Herewe use transmission electron microscopy, electron diffractionpatterns and rockmagnetic analyses to assess the origins ofnanometre-scale greigite crystals found in Pliocene claystonesfrom the Carpathian foredeep of Romania. We find that, likemodern magnetosomal greigite grains, the crystals are singledomain8, with few crystallographic defects and an overall shapeconsistent with an intracellular origin. We suggest these crystalsare magnetosomal in origin, which would place them amongthe oldest greigite magnetofossils identified so far. The crystalsalso carry a primary magnetic signal, which has remained stablesince its acquisition 5.3–2.6 million years ago. We suggest thatgreigite magnetofossils could therefore provide reliable recordsof ancient geomagnetic field variations, and that they could alsobe used as a proxy to assess palaeoenvironmental conditions inlow-oxygen sedimentary environments.
Robust fossil evidence for magnetite magnetofossils dates backto the Cretaceous period9, whereas claims of magnetofossils extendback to the early Proterozoic era10 (∼2 Gyr). Today, these bacteriaare cosmopolitan in distribution and easy to identify in modernenvironments, where they contribute to the biogeochemical cyclingof important elements, including iron, nitrogen, sulphur andcarbon7. These crystals exhibit high chemical purity, specific crystalmorphologies and exceptionally narrow grain-size distribution8,11.
Magnetotactic bacteria achieve directional sensing usingmagnetosomes, which are membrane-bounded chains offerrimagnetic crystals. Two magnetic minerals have beenunequivocally recognized to be produced by magnetotacticbacteria: magnetite1,2 (Fe3O4) and greigite3–5 (Fe3S4).Magnetosomal minerals dominantly form around the oxic–anoxicinterface in aquatic habitats7, reflecting the palaeo-redox conditionsand are of interest for geochemistry and geobiology. Theyare of importance also for palaeomagnetism because, whenpreserved, they can significantly contribute to the primarynatural remanent magnetization (NRM) of sedimentary rocks.
Magnetosomal magnetite is often well preserved and regularlyobserved in geological archives (for example, see refs 9,10). Greigitemagnetosomes have been uncontestedly identified only in recentsoils and lake sediments, although their occurrence has also beenclaimed in Miocene rocks of the Western Carpathian foredeep12.
Authigenic greigite has been known since 1964 (ref. 13) andis preserved in rocks at least as old as the Cretaceous14. However,the reliability of palaeomagnetic data from greigite-bearing rocksis frequently questioned15 because greigite is thermodynamicallymetastable16 and the timing of NRM acquisition by greigite isnot well constrained because of its diagenetic formation15. It wasfurther assumed that greigite would not last long in the geologicalrecord because excess sulphur would cause transformation topyrite16. A recent re-evaluation of greigite’s thermodynamics17,however, suggests that, despite its metastability, greigite maypreserve a primary NRM for geological times14.
Recent greigite-based magnetostratigraphies straightforwardlycorrelate to the geomagnetic polarity timescale18,19 and supportthe formation and preservation of ancient greigite in sedimentaryrocks20. These records come from the Carpathian foredeep ofRomania (Fig. 1), which was part of the Eastern Paratethys(see Supplementary Information, Fig. S1), a large semi-isolatedfresh to brackish-water domain that comprised the present-day Black Sea and Caspian Sea regions18. Large quantities ofdetrital material derived from the uplifted orogen and activevolcanic sources were deposited in shallow-water environmentswith ostracods and molluscs indicative of the euphotic zone21,22.Posfai et al.12 previously conducted a transmission electronmicroscopy (TEM) study of greigite from one sample from Poland’sMiocene Carpathian foredeep and concluded, solely on the basisof analysis of particle size and shape distributions, that thesediment might contain crystals produced by the multicellularmagnetotactic prokaryote.
Thermomagnetic measurements in air, acquiredgyro-remanence during alternating field demagnetization (seeSupplementary Information, Fig. S2) and scanning electronmicroscopy showed that greigite is the key magnetic mineral inthe sedimentary rocks of the Romanian Carpathian foredeep20.Positive reversal tests, a positive fold test and the occurrence ofinclination shallowing (Fig. 1e,f) provided further evidence for anearly acquisition of the NRM20.
Figure 1 Greigite-based magnetostratigraphy of the Badislava valley (central plots). Circles and triangles represent high-temperature (HT) and low-temperature (LT)components, respectively. Shaded bands indicate intervals of delayed low-temperature acquisition. a, Thermomagnetic run for greigite-bearing samples.b–d, Demagnetization diagrams illustrating the transition from reversed (d) to normal polarity (b) via a sample (c) recording two antipodal directions. e,f, Histograms ofinclinations on using the elongation/inclination (E/I) correction method29. Coloured lines refer to expected (IncGAD, yellow), original (Incorg, blue), unflattened (IncEI, green) andmost frequent bootstrapped (red, with 95% error bounds: dashed red lines) mean inclinations.
An earlier scanning electron microscopy study on theRomanian rocks20 revealed octahedral greigite crystals of aninorganic origin that range 400–1,000 nm in size. The number ofgreigite particles, however, was remarkably small when comparedwith the high initial intensity of the samples (10–65 mA m−1).Consequently, the presence of an extra magnetic carrier in a smaller(magnetofossil) grain-size range was suspected. To identify theprecise nature of greigite formation in these rocks, we used acombination of mineral magnetic methods and TEM. In addition,we evaluated our results using the six criteria for magnetofossil
identification of Kopp and Kirschvink23: (1) the contextual andpalaeomagnetic evidence for a primary origin, (2) the presenceof a significant single-domain magnetic phase, (3) size and shapedistributions characteristic of magnetosome crystals, (4) evidencefor chains of crystals, (5) evidence for chemical purity and(6) high-resolution TEM (HRTEM) evidence for crystallographicperfection. Our earlier palaeomagnetic and palaeoenvironmentalresearch of the Carpathian foredeep fulfilled the first criterion. Theother five criteria require an extensive TEM study combined withrockmagnetic experiments. For TEM imaging, we used magnetic
Figure 2 Fossil elongated prismatic greigite magnetosomes. a, TEM micrograph of a prismatic, slightly elongated {100}+{111} greigite crystal, typical ofmagnetosomes, very close to the idealized crystal habit (inset). b, HRTEM detail of the greigite crystal. The inset shows well-ordered lattice fringes from the area in thedashed square. c, EDS from the crystal with distinct Fe and S peaks; O, Al and Si are from the background signal of the clay flake; Cu peaks originate from the TEM grid.d, Selected-area electron diffraction pattern with the same orientation as b. b and d were recorded with 41◦ -tilt difference from a.
concentrates obtained from approximately 20 g of powdered rocksamples (see Supplementary Information).
TEM analyses on these extracts identified numerousnanoparticles (Figs 2a, 3a,b and Supplementary Information,Figs S3,S4) that seemed to be chemically pure and have fewcrystallographic defects, passing two criteria (chemical andcrystallographic perfection)23. The crystals span a grain-sizerange of 20–75 nm, implying that they are magnetically singledomain, although smaller, probably superparamagnetic grains werealso distinguished. Many of the particles are irregular in shape,but exhibit strong diffraction (Fig. 3a), indicating that they arehighly crystalline. Other particles show elongated (Fig. 2a andSupplementary Information, Fig. S3) and hexagonal (Fig. 3a)outlines when viewed in projection, which is characteristic ofelongated prismatic and truncated cuboctahedral grains and pointsto cubic crystal symmetry. Energy-dispersive X-ray spectroscopy(EDS) analysis shows that most of particles consist of iron andsulphur (Figs 2c and 3c). HRTEM (Fig. 2b) and single-crystalselected-area electron diffraction patterns (Fig. 2d) indicate thatthe measured d-spacing corresponds to those of greigite. The size
distribution of 20–75 nm, the elongated prismatic or cuboctahedralcrystal morphologies and the elemental composition all indicatethat these greigite crystals have a magnetosomal origin. The roughlyprismatic (Fig. 2a and Supplementary Information, Fig. S3)and cuboctahedral (Fig. 3a,b) magnetosomes are magneticallysingle domain (see Supplementary Information, Fig. S4) andwould have been responsible for the magnetotactic reactionof the living organism4. Isothermal remanent magnetizationcomponent analysis revealed a very small dispersion parameterof approximately 0.10–0.15 log units20, which is also indicative of amagnetosomal origin of the magnetic crystals12. The single-domaingreigite with the grain-size distribution and shape typical ofmagnetofossils, having truncated-edge crystal morphology, passestwo more magnetofossil identification criteria23.
The last and most difficult to fulfil criterion in rock records isthe presence of magnetosomal chains, because both diagenesisand magnetic extraction techniques can contribute to chaindisruption24. We identified a few single-domain magnetitemagnetosomes (see Supplementary Information, Fig. S5),although their contribution to the NRM is minimal because
Figure 3 Fossil cuboctahedral greigite magnetosomes. a, TEM micrograph ofgreigite crystals; some are close to a zone-axis orientation producing strongdiffraction contrasts. b, Magnification shows the cuboctahedron {100}+{111}crystal morphology found in both magnetite and greigite magnetosomes; manyparticles have well-defined edges. The inset represents the idealized crystal habit.c, EDS from crystals in b; see also caption to Fig. 2. The intensity of S and Fe peaksis lower than that of the Cu peaks because of the very small crystals and/orpositioning of the material near the copper bars of the grid, catching morestray radiation.
the samples are demagnetized below 400 ◦C. We conclude thatour greigite magnetofossils pass five out of six criteria formagnetosome identification23.
Our Carpathian samples thus comprise two distinctly differenttypes of greigite, generated by two different formation mechanisms(Fig. 1a): (1) small (20–75 nm) slightly prismatic elongated andcuboctahedral crystals of magnetosomal origin and (2) largeroctahedral grains (400–1,000 nm) of authigenic origin. Close topolarity reversals, the thermal demagnetization diagrams showthe presence of two different (even antipodal) NRM componentsin a single specimen (Fig. 1b–d). Unexpectedly, the hysteresisloop and the first-order reversal curves (see SupplementaryInformation, Fig. S6) indicate only a unimodal coercive forcedistribution, which is unusual for a specimen recording twodifferent directions. We therefore fitted the isothermal remanentmagnetization acquisition curve25, with two magnetic componentshaving approximately the same mean acquisition field (B1/2) buta significantly different dispersion parameter (see SupplementaryInformation, Fig. S6). This translates into two different grain-sizedistributions, having the same mean coercivity. Magnetosomes areknown for their narrow coercivity switching field distribution (lowdispersion parameter)12 and therefore we tie the narrow dispersionparameter in our samples to the greigite magnetosomes. The widerdistribution would thus be related to the authigenic phase ofgreigite. We acknowledge that authigenic greigite has a narrowgrain-size distribution26 (when compared with other magneticminerals), but magnetosomal greigite has even lower dispersionparameter values than the authigenic greigite phases. First-orderreversal curve analysis27 of thermally treated samples shows thatgreigite survives up to 350 ◦C and is replaced at ∼360 ◦C, by a non-magnetic phase13. This behaviour is consistent with the thermaldemagnetization spectra of our samples, indicating that greigitewas indeed the NRM carrier.
Authigenic or early diagenetic greigite formed later than themagnetosomes, deeper in the sediment and therefore acquireda later magnetic field. The delayed NRM acquisition is easilyobservable and directionally traceable from the demagnetizationdiagrams, especially in the intervals that straddle polarityreversals (Fig. 1). The low-temperature component must beattributed to diagenetic greigite because it records the delayedcomponent (Fig. 1c and Supplementary Information, Fig. S7). Thehigh-temperature component represents greigite magnetosomes,which formed close to the sediment–water interface7 or in thewater column28 at the time of the deposition and thus record themagnetic field without significant delay. Generally, larger grainsresist thermal demagnetization and, in the case of greigite, thermalalteration longer. Here, the ∼10 times smaller magnetosomeswith their high chemical purity and few crystallographic defectsseem to persist to the highest temperatures. The larger, diageneticpseudo-single-domain greigite particles would have a less stablemagnetization, explaining partially why the larger fraction isless resistant to thermal demagnetization than the smaller one.The origin of the two components is furthermore confirmed bytheir different inclination values distinguishable in the thermaldemagnetization diagrams. We obtain mean inclinations of52.0◦ for the high-temperature (Fig. 1e) and of 60.4◦ for thelow-temperature component (Fig. 1f). This implies that inclinationshallowing has significantly affected the high-temperaturecomponent (Fig. 1e), caused by dewatering and compaction of thetop sediment layer. In contrast, no significant inclination error isobserved for the low-temperature component (Fig. 1f), because theauthigenic greigite forms later in the sediment, when compactionhad largely come to an end. Applying the inclination errorcorrection method using the field model TK03.GAD (ref. 29) onboth data sets corrects the high-temperature and low-temperatureinclinations to 65.5◦ and 64.9◦, respectively. Both corrected valuesare remarkably similar and indistinguishable from the expectedinclination at the site latitude (IGAD = 63.6◦).
Palaeomagnetism is widely used in earth sciences for platetectonic reconstructions, for dating and correlation of marineand continental sequences and for studying geomagnetic fieldbehaviour. Here, we show that magnetosomal greigite can survivegeological times and that a primary NRM component canbe extracted, noticeably enhancing the value of greigite forpalaeomagnetic studies, including records of rapid geomagneticvariations. We emphasize the importance of small demagnetizationsteps in the 300–360 ◦C temperature range, because magnetosomalgreigite survives heating up to 350–360 ◦C, whereas authigenicgreigite is removed at 290–300 ◦C.
In some conditions, greigite magnetosomes may have agreater preservation potential than magnetite magnetosomesbecause the latter ultimately dissolve under anoxic conditionswhereas the former persist—having been formed under suchconditions. Greigite magnetofossils might be expected to be moreabundant in higher productivity, more sulphidic sediments, butthese environments are still insufficiently studied23. The greigite-producing bacteria prefer reduced conditions and are probablyanaerobic sulphate reducers. The high preservation capacityof greigite magnetosomes may help to detect environmentalvariations, expressed by biogeochemical changes in sedimentarybasins. The magnetofossil record may serve as tracers of localchanges in oxygen level and provide an underexploited archive ofthe long-term evolution of marine redox stratification importantin characterizing anoxic/euxinic sedimentary environments such asthe Oceanic Anoxic Events.
Received 28 April 2008; accepted 26 September 2008; published 19 October 2008.
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Supplementary Information accompanies the paper at www.nature.com/naturegeoscience.
AcknowledgementsThis work was financially supported by the Netherlands Research Centre for Integrated Solid EarthSciences (ISES) and the Netherlands Geosciences Foundation (ALW) with support from theNetherlands Organization for Scientific Research (NWO). J. Kirschvink is thanked for providing thenew code for the single-domain stability field of greigite.
Author contributionsI.V. initiated the project, undertook the analyses and provided the interpretation. C.F. and J.D.M.assisted and advised on TEM microscopy. C.G.L. assisted with the NRM analyses and the TK03.GADcorrection. M.J.D. and W.K. advised and assisted throughout.
Author informationReprints and permissions information is available online at http://npg.nature.com/reprintsandpermissions.Correspondence and requests for materials should be addressed to I.V.