A perfect (geochemical) storm yielded exceptional fossils in the early ocean

Timothy W. Lyons1 Department of Earth Sciences, University of California, Riverside, CA 92521

he geologic record treats us to rare examples of dazzling pre- T servation of fossil animal remains. None is more spectac- ular than the faithful traces of even the most delicate soft tissues that are best and most commonly expressed during the early and middle parts of the Cambrian Period approximately 540 to 500 Mya and epito- mized by the famous Burgess Shale in British Columbia (Fig. 1). Models for the mechanisms behind such extraordinary soft-tissue fossilization abound. The problem, though, is that most invoke conditions, such as rapid deposition beneath oxygen-poor seawater, that are far more common through time than the Fig. 1. Arthropod fossil from the Burgess Shale described by C. D. Walcott in 1912 as Sidneyia inex- special fossils themselves. Now, Gaines pectans (named in honor of his son, Sidney). The beautiful traces of soft tissue preserved as carbona- fi et al. (1) tackle this conundrum by taking neous lms include the feathery gill structures seen readily in the photograph. The Burgess Shale, the most famous of the Cambrian fossil deposits, is marked by exceptional preservation of soft tissue, in- a decidedly nonuniformitarian view of the — cluding remarkable records of soft-bodied organisms lacking skeletal remains. (Image is in the public global Cambrian ocean asserting that domain; from ref. 9.) chemical conditions came together to yield an unusual if not unique preserva- tional window. weathered core material is particularly unless sulfate was scarce in that early We have all seen a rotting jellyfish on well suited to geochemical analysis. seawater. the beach or festering road kill along the Their perspective on ancient organic Perhaps the most important insight highway. Bacteria are fast-acting and decay builds, as it must, on a generation of proffered by Gaines et al. (1) lies with the ubiquitous, and so the preservation of pioneering research in the laboratory suggestion that the exceptional Burgess soft tissue—fossil remains other than and modern ocean. These lessons have Shale-type preservation is indeed a mani- hard bones or shells such as guts and taught us that the currency in the energy- festation of low sulfate concentrations in gills—requires something out of the ordi- yielding processes of bacterial metabo- the Cambrian ocean. Seawater sulfate nary. Rapid entombment on the seafloor lisms lies with the electrons transferred concentrations at only a small fraction of ’ helps, as by the large amounts of mud during oxidation of organic remains today s are a common theme in studies of kicked up by storms and underwater the Precambrian ocean more than 540 (i.e., electron loss), and O2 is the most fl avalanches known as turbidites, which energetically favorable electron acceptor Mya, re ecting a sequence of bacterial bury the rotting remains away from the and thus facilitator in the rapid loss of soft sulfate reduction and subsequent forma- − tion of pyrite (FeS ) when the resultant bacteria-favoring oxygen in the overlying tissue (3). However, sulfate (SO 2 ) is also 2 4 hydrogen sulfide reacted with iron seawater. An ocean poor in dissolved abundant in modern seawater, second only O in the deeper waters would help, and − (reviewed in ref. 5). Pyrite burial is ulti- 2 to Cl among the anions, and many bac- mately a sink for sulfate and prospers such conditions may have abounded dur- teria can efficiently oxidize (i.e., degrade) ing the Cambrian (2). when large portions of the deep ocean are organic remains by reducing sulfate to O -free, as has been suggested for most, if From a platform of past experience and hydrogen sulfide (H S) in the process. In 2 new data, however, Gaines et al. (1) re- 2 not all, of the Precambrian (6). Today, fact, in many coastal settings in the mod- such conditions are limited to small areas mind us that even rapid burial under ern ocean, as much organic decay happens oxygen-free waters is not enough to of the ocean (much less than 1%), with the through bacterial sulfate reduction as explain the extraordinary preservation of Black Sea being our best example. How- through aerobic (i.e., O -related) pro- “Burgess Shale-type” fossils. They specif- 2 ever, recent work is pointing to a reprise of ically refined their perspectives on cesses (4). In a competitive sense, aerobic the widespread anoxia of the Precambrian fossil preservation through detailed geo- decay is more energetically favorable, but during the Cambrian (2), and low con- chemical and sedimentological analysis of burial within the sediments isolates the centrations of seawater sulfate may have many of the world’s spectacular Burgess decaying organic matter from the over- been the result. Shale-type fossils and their host rocks, in- lying source of O2. The big difference be- Gaines et al. (1) support this assertion cluding the Burgess Shale proper, which C. tween the two pathways is that abundant of low sulfate availability with independent D. Walcott of the Smithsonian Institution bacterial sulfate reduction only occurs discovered a century ago. Also included in anaerobically, in the absence of oxygen. the analytical mix is new drill core from We are left with the distinct possibility that Author contributions: T.W.L. wrote the paper. the Chengjiang interval of the Early soft tissue could have been consumed The author declares no conflict of interest. Cambrian Yu’anshan Formation near quickly even when faced with rapid burial See companion article on page 5180. 1 Haikou, Yunnan, China. Fresh, un- beneath an O2-lean Cambrian ocean— E-mail: [email protected].

5138–5139 | PNAS | April 3, 2012 | vol. 109 | no. 14 www.pnas.org/cgi/doi/10.1073/pnas.1202201109 Downloaded by guest on September 29, 2021 COMMENTARY

evidence that lies with the sulfur isotope beds point to rapid deposition and, quite factors, they argue, led collectively to composition of pyrite at the Chengjiang likely, early cementation. (Compaction low amounts of anaerobic decay (i.e., in fl locality in China. Bacteria not only reduce during burial can otherwise atten out absence of O2). sulfate to hydrogen sulfide, but they do the random, “house-of-cards” structures At the end of the day, Gaines et al. (1) so with a strong preference for the light with which clays typically start.) Also, posit a perfect storm of taphonomic 32 sulfur isotope, S, compared with the reworked slump deposits that formed pe- conditions expressed perhaps universally 34 32 heavier S. Enrichments in S in the re- necontemporaneously with sediment de- among the many globally distributed sulting pyrite are a telltale sign of bacterial position show signs of very early, preslump localities of Burgess Shale-type fossil sulfate reduction under sulfate-replete cements, and their arguments are consis- preservation of approximately the same conditions. When sulfate becomes limit- tent with carbon isotope data that suggest age: low sulfate in the ocean along with ing, however, something very different a seawater source for most of the cement. high carbonate saturation states that happens: the bacteria lose much, if not favored almost immediate cementation of all, of their ability to distinguish between At the end of the day, sediments deposited rapidly beneath an 32S and 34S when reducing sulfate—in the oxygen-poor ocean. Rapid deposition and extreme case when they reduce it all. Gaines et al. posit a Pyrite with 34S/32S ratios approaching widespread ocean anoxia are common those of the starting sulfate of the global perfect storm of features over the history of animal life, yet ocean suggests that sulfate was in limited spectacular fossils are typically not the supply, and this is just what Gaines et al. taphonomic conditions. result. In the minds of Gaines et al., the observe in China (1). “just-right” chemical conditions in the There is one more chapter in this story. ocean delivered the silver bullet. Sulfate, even when present in small The surface cement could have provided We might be inclined to argue that such amounts in the ocean, can diffuse from a cap that inhibited further transport of serendipity is too much to hope for, seawater into the sediments, sustaining sulfate into the sediment layers below but the response would be that extraordi- anaerobic decay of soft tissue and frac- and thus restricted further anaerobic de- nary fossils are extraordinarily rare and tionating sulfur isotopes in the process. cay of the associated organic remains, never the children of typical con- This possibility also occurrs to Gaines which were buried rapidly beneath an ditions. We might also argue that the et al. (1). The final step, then, demands O2- and sulfate-lean ocean. necessary ocean chemistry requires further fi a control that might have limited the Gaines et al. (1) are not the rst to study. For example, could carbonate fl diffusional ow of sulfate from the express their opinions on the special cementation really have been fast fl seawater into the pore uids within the conditions required to preserved carbo- and pervasive enough to stifle decay so fl sediments that covered the sea oor. One naceous traces of soft tissue in Burgess effectively? How low was sulfate in the fl possibility for restricting ow is very Shale-type fossils. Indeed, these fossils and Cambrian ocean, and was it low enough to their special preservation are among the early and rapid cementation of those inhibit decay (8)? Regardless, Gaines et al. sediments by calcium carbonate pre- most talked-about themes in studies of (1) give us key observations and geo- cipitated from an ocean with a high state taphonomy—the science that deals with chemical data and build on a foundation of saturation with respect to carbonate the postmortem transformation of decay- minerals such as calcite and aragonite. ing remains in soft mud to fossils pre- laid from a large body of past work, in- Past studies of the Cambrian ocean have served in rocks over many millions of cluding their own, that all point to the suggested unusually high alkalinity that years. However, by looking for common possibility of a perfect storm. may have favored rapid and pervasive themes among the deposits, generating It is our good fortune that ocean formation of early calcium carbonate new geochemical data, and tying the evolution may have given us a very special cements on or just below the seafloor observations to the best estimates of physio-biogeochemical window to view (e.g., ref. 7), and Gaines et al. (1) bring chemistry in the Cambrian ocean, they the early diversification of animal life their own evidence for this condition to provide unique insight—in particular, the across the globe—but perhaps it did the table. The random orientations of purported relationships to hypothesized so uniquely and narrowly in time over tabular, microscopic clay minerals that low sulfate conditions and high levels of the approximately half billion years of they observed in Burgess Shale-type fossil calcium carbonate saturation. These animal history.

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