COMMENTARY

Big discovery for biogenic

Peter C. Lippert1 Earth and Planetary Sciences Department, University of California, Santa Cruz, CA 95064

ne of the most significant temperature-dependent fractionation of rarely exceed a few hundred nanometers characteristics of the Anthro- oxygen isotopes between cultured bio- and most are less than 120 nm. In con- pocene (the present age of genic magnetite crystals and the water trast, individual magnetite particles discov- geologic time) is the rate at from which those crystals precipitated ered by Schumann et al. (4) range from 1 Owhich humans are perturbing the global to 4 micrometers in length. These dimen- (5). Using nanometer-scale secondary carbon cycle. The potency of carbon ion mass spectroscopy (NanoSIMS), sions are similar to or exceed the cellular dioxide and methane as greenhouse Schumann et al. (4) measured oxygen size of most common aquatic bacteria, gases and their effects on Earth’s tem- isotope compositions in magnetofossils leading the authors to suggest these large perature balance is well established (1), that are consistent with independent crystals were produced by eukaryotes. and the myriad of climate and ecologi- paleotemperature estimates of marine Exceptionally large prokaryotes (cellular cal changes and feedbacks in response waters during the PETM (6). Although diameters up to 750 ␮m) replete with sul- to this abrupt warming is the focus of the utility of the NanoSIMS results pre- fur or calcite inclusions are common in much ongoing research (1, 2). The geo- sented here is compromised by their low some high-productivity shelf sediments logic record is one of our greatest assets precision, they lead the way in the de- (13, 14), however, suggesting that these in understanding the short- and long- new forms of magnetofossils may be term environmental responses to ex- unique environmental adaptations of pro- treme fluctuations in the carbon cycle, Most magnetofossils karyotes and not necessarily eukaryotes. and the Paleocene–Eocene Thermal Thus, a key question is what function did Maximum (PETM), which occurred Ϸ55 are produced by these magnetofossils serve? Are they skel- million years ago, is an ideal analogue etal elements or part of a defensive cara- for the Anthropocene. The PETM is various species of pace (4), or are they analogous to sulfur marked by an abrupt negative carbon inclusions in giant sulfur-reducing bacteria isotope excursion that indicates a mas- . (13) and function as batteries for the or- sive injection of light carbon into the ganism’s iron-based metabolism? Al- oceans and atmosphere over a period of though their function remains enigmatic, a few thousand years. This perturbation velopment and application of this under- the environmental implications of these to the carbon cycle resulted in super- utilized marine paleothermometer and abundant and unique magnetofossils are greenhouse conditions that persisted for bolster the evidence for abundant and nonetheless significant. as long as 180,000 years. Mean annual unique biogenic magnetite in PETM-age Magnetotactic bacteria commonly live temperatures and deep and surface sediments. in the oxic–anoxic transition zone of ocean temperatures at all latitudes rose The discovery of magnetofossils in fresh, brackish, and marine aquatic by 5–8°C (3). Terrestrial plants and PETM-age marine sediments is not new, environments where dissolved oxygen mammals diversified and radiated, and however. Two independent studies (7, 8) and sulfide are low and bioavailable new marine microorganisms evolved and recently demonstrated that the unusual iron is high [see review by Kopp and flourished while others disappeared for- abundance of Ϸ30- to 120-nm-sized Kirschvink (12)]. These environments ever. In this issue of PNAS, Schumann magnetite (Fe O ) particles in PETM- include suboxic sediments and seasonally- et al. (4) report evidence for new micro- 3 4 age sediments from several drill cores stratified euxinic estuaries and freshwater organisms that appeared and disap- lakes. The co-occurrence of these newly peared with the PETM, signaling from New Jersey (9) was produced by magnetotactic bacteria. Rock magnetic discovered magnetofossils with abundant another specific ecological response to conventional magnetofossils suggests the the biogeochemical changes associated data from similar studies on marine sed- iments from New Zealand (10) and organisms that synthesized them share a with this extreme warming event. similar ecological niche. Most magnetofos- Using high-resolution transmission Egypt* are consistent with the occur- rence of magnetofossils at these locales sils are removed from the geologic record electron microscopy and nanometer- by reductive dissolution with burial under scale chemical analyses, Schumann et al. as well. What is remarkable about the steady-state redox conditions. Increased (4) found exceptionally well-preserved, findings of Schumann et al. (4) is the sedimentation rates or nutrient supply and uniquely-shaped stoichiometric magne- size and morphology of the magnetofos- productivity, however, lead to nonsteady tite (Fe O ) particles in PETM-age ma- sils, which are unlike any previously 3 4 redox conditions and suboxic sediments at rine sediments from a drill core from reported. a depth that fosters magnetite preserva- New Jersey. The elongate prism and Most magnetofossils are produced by tion. Thus, the restrictive ecological niche spearhead morphologies are unlike any various species of magnetotactic bacteria magnetite crystals previously reported that biomineralize cubic, cubo-octahedral, or bullet-shaped magnetite or greigite and are inconsistent with a hydrother- Author contributions: P.C.L. wrote the paper. mal, volcanogenic, or diagenetic origin. (Fe2S4) crystals called (11, The author declares no conflict of interest. Instead, the crystal morphologies are 12). Magnetosomes are typically arranged most consistent with a biogenic origin. in elongate chains within the cell to orient See companion article on page 17648. 1 In addition to the discovery of large the organism along magnetic field lines to E-mail: [email protected]. and unique forms of biogenic magnetite, aid the organism’s search for nutrients *Tikoo SM, et al. (2007) Testing the Paleocene-Eocene Ther- mal Maximum magnetofossil spike hypothesis. American Schumann et al. (4) present the first ap- and might even be used as an intracellular Geophysical Union Fall Meeting, December 10–14, 2007, plication of fossilized biogenic magnetite energy or iron supply (12). Although San Francisco, CA, Eos Trans AGU 88(Suppl), abstr B31D- (magnetofossils) as a paleothermometer. these chains can reach several hundred 0619. Previous studies demonstrated the nanometers in length, individual particles © 2008 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0809839105 PNAS ͉ November 18, 2008 ͉ vol. 105 ͉ no. 46 ͉ 17595–17596 Downloaded by guest on September 27, 2021 occupied by magnetotactic bacteria as well to exploit and tolerate periods of high bearing sediments may be necessary to as their preservation as magnetofossils and low nutrient availability, such as fully evaluate the environmental condi- makes them useful biomarkers for envi- the dinoflagellate Apectodinium (e.g., tions on the North American continen- ronmental change. ref. 19) or even an iron-metabolizing tal shelf during the PETM. But what does this mean for the equivalent to the giant sulfur bacterium Furthermore, are the environmental PETM specifically, and for rapid global Thiomargarita (13). conditions that spurred the magnetotac- warming events in general? The PETM- The New Jersey magnetofossil record tic bacteria bloom and the diversifica- age sediments from the New Jersey (4, 7, 8) clearly indicates high bioavail- tion of iron biomineralizing organisms cores were deposited in subtropical ability of iron on the Atlantic coastal specific to the New Jersey continental near-shore waters on the shallow conti- plain during the PETM. High magneto- margin or the subtropics in general, or nental shelf (15). Moreover, a proximal abundance and diversity are coin- are they globally extensive? Rock mag- deltaic system could deliver nutrient-rich cident with increased kaolinite deposi- netic and microscopy results from the sediment from the North American con- tion (20), abundant high-productivity few PETM sections that have been in- tinent onto the shelf (15). The rapid nannoplankton (21) and dinoflagellate vestigated for the occurrence of biogenic warming associated with the onset of (19) assemblages, and increased accu- magnetite (7, 8, 10, *, †) suggest the the PETM caused significant changes in mulation rates of organic and inorganic magnetofossil spike may be global, al- the hydrologic cycle, with a shift toward carbon (18) on the New Jersey shelf. though limited to the shallow continen- stronger seasonality during the PETM. These observations indicate significant tal shelves and most pronounced along These changes would have been pro- changes in biogeochemical cycling, and the eastern North American continental nounced in the subtropical evaporative by extension productivity, on the conti- margin. With the discovery of anoma- belts (e.g., see refs. 6, 16, and 17) where nental shelf. lously large and unique magnetofossils, the New Jersey sediments were depos- What remains unresolved at this point Schumann et al. (4) emphasize not only ited (7) and are consistent with records is the extent to which biologic productiv- the sensitivity of continental shelf eco- of enhanced continental weathering and ity increased and possibly functioned to logical communities to abrupt warming, episodic sediment flux to the coastal sequester carbon on the continental but also that the evidence for such dras- oceans (e.g., refs. 17 and 18). Thus, shelves. Did shallow continental marine tic changes is considerably larger than strong seasonality would have estab- waters and sediments remain suboxic or we expected. lished highly-stressed environments on did they episodically become euxinic? the continental shelves in which short Schumann et al. (4) provide a compel- episodes of high nutrient availability ling argument in favor of suboxic condi- †Lippert PC, Zachos J, Bohaty S, Quattlebaum T (2004) Rock punctuated longer, nutrient-lean periods. tions, but additional geochemical studies magnetic properties across Paleocene-Eocene boundary These variable environmental conditions that establish the organic carbon con- sediments from the North Atlantic, South Atlantic, and Eastern Pacific. American Geophysical Union Fall Meeting, would favor the diversification and pro- tent, sedimentary redox conditions, and December 13–17, 2004, San Francisco, CA, Eos Trans AGU liferation of robust organisms adapted paleoproductivity of the magnetofossil- 85(Suppl), abstr GP31B-0840.

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