Current Biology Magazine cyanobacteria today? Certainly, it Across these geological timescales, would be diffi cult to assume that it is important to be frank about the The Neoproterozoic cyanobacteria have not changed many large gaps we have in our morphologically in over 3 billion years. understanding of the evolutionary Nicholas J. Butterfi eld Although there are many lines of succession of life. Truly, it is remarkable evidence suggesting that life arose how much we have already been able The Neoproterozoic era was arguably during the Archean, it is important to to piece together through varying fi elds the most revolutionary in Earth history. highlight the uncertainty surrounding spanning biology, paleontology, and Extending from 1000 to 541 million Archean microfossils as evidence of geosciences. The diffi culty in studying years ago, it stands at the intersection early life. these ancient questions should not of the two great tracts of evolutionary Other lines of evidence have stemmed deter us from studying them, but rather time: on the one side, some three from molecular fossils — the presence inspire us to continually fi nd alternative billion years of pervasively microbial and identifi cation of complex organic ways of studying them in order to test ‘Precambrian’ life, and on the other biological molecules (i.e., biomarkers) in prior assumptions about the robustness the modern ‘Phanerozoic’ biosphere sediments, used to date the existence of of previous hypotheses. If anything, with its extraordinary diversity of large certain organisms. Biomarkers make the advances in our understanding of early multicellular organisms. The disturbance assumption that molecules could only life will be interesting in light of newly doesn’t stop here, however: over this have been produced by certain lineages. developed techniques and the growing same stretch of time the planet itself was Ideally, biomarkers would provide the abundance of sequence data to begin in the throes of change. Tectonically, chemical fi ngerprints necessary to testing assumptions we have had with it saw major super-continental identify the microbes living in ancient us for decades. reconfi gurations, climatically its deepest sediments. This assumption has been ever glacial freeze, and geochemically challenged with the gradual acceptance some of the most anomalous of the fact that lateral gene transfer is FURTHER READING perturbations on record. What lies behind nearly ubiquitous across all bacteria. this dramatic convergence of biological Canfi eld, D.E. (2014). Oxygen: A Four Billion Year Correspondingly, some of the most History (Princeton: Princeton University Press). and geological phenomena, and how important cyanobacterial biomarkers Canfi eld, D.E., and Teske, A. (1996). Late exactly did it give rise to the curiously (i.e., 2-methylhopanes) have been Proterozoic rise in atmospheric oxygen complex world that we now inhabit? concentration inferred from phylogenetic and shown to be present in other bacterial sulphur-isotope studies. Nature 382, 127–132. Like all historical reconstructions, phyla. This example highlights how our Dalton, R. (2002). Microfossils: Squaring up over any useful study of the Neoproterozoic ancient life. Nature 417, 782–784. incomplete understanding of extant life Des Marais, D.J. (2000). When did photosynthesis requires a chronological framework can easily alter our interpretations of emerge on earth? Science 289, 1703–1705. to keep things in order (Figure 1). ancient life. Johnston, D.T., Wolfe-Simon, F., Pearson, A., and To a fi rst approximation, the fi rst Knoll, A.H. (2009). Anoxygenic photosynthesis It is impossible to get away from modulated Proterozoic oxygen and sustained half of the era — the Tonian — uncertainty when examining the Earth’s middle age. Proc. Natl. Acad. Sci. USA appears to represent Proterozoic 106, 16925–16929. evidence for early life. This is just the Johnson, J.E., Webb, S.M., Thomas, K., Ono, business as usual, a continuation nature of the subject matter. With this in S., Kirschvink, J.L., and Fischer, W.W. (2013). of the Mesoproterozoic status quo. mind, it becomes even more important Manganese-oxidizing photosynthesis before the Evidence from microfossils (Figure rise of cyanobacteria. Proc. Natl. Acad. Sci. USA to understand the challenges and 110, 11238–11243. 2A,F,G), chemical fossils (primarily nuances in interpreting the evidence Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., lipid biomarker molecules) and used in generating further hypotheses and Worm, B. (2011). How many species are sedimentology (stromatolites and other there on Earth and in the ocean? PLoS Biol. 9, on early life. e1001127. microbial mat fabrics) point to on-going Novacek, M.J. (2001). The Biodiversity Crisis: Losing monopolization of marine productivity What Counts (New York: The New Press). Conclusion Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, by cyanobacteria, while geochemical Phototrophy has sustained life on D., McGoldrick, P., Rainbird, R.H., Johnson, T., proxies document extensively stratifi ed Earth, possibly since the dawn of life. Fischer, W.W., and Lyons, T.W. (2014). Low Mid- oceans with free oxygen limited largely Proterozoic atmospheric oxygen levels and the Archean ecosystems were most likely delayed rise of animals. Science 346, 635–638. to its sun-lit surface layers. Tonian-age sustained by anoxygenic phototrophic Rashby, S.E., Sessions, A.L., Summons, R.E., eukaryotes are recognizable in the form organisms which may have grown in and Newman, D.K. (2007). Biosynthesis of sterane biomarkers and protistan- of 2-methylbacteriohopanepolyols by an stromatolites much like modern day anoxygenic phototroph. Proc. Natl. Acad. Sci. grade microfossils (Figure 2B–D,H,I), microbial mats. With the innovation of USA 104, 15099–15104. but show little inclination to diversify Shih, P.M., and Matzke, N.J. (2013). Primary the oxygen-evolving complex, oxygenic endosymbiosis events date to the later or expand their decidedly marginalized photosynthesis provided the biological Proterozoic with cross-calibrated phylogenetic Mesoproterozoic footprint. There is catalyst to accumulate oxygen in dating of duplicated ATPase proteins. Proc. Natl. no sign of multicellular animals or Acad. Sci. USA 110, 12355–12360. the atmosphere. These metabolic land plants at this stage, and rates of inventions provided profound shifts in evolutionary turnover are fundamentally how once purely abiotic geochemical 1Joint BioEnergy Institute, 5885 Hollis lower than in the subsequent fossil 2 cycles would integrate the evolution St, Emeryville, CA 94608, USA. Physical record. The supercontinent Rodinia Biosciences Division, Lawrence Berkeley of life to ultimately transform into the National Laboratory, One Cyclotron Rd, begins to break up in the middle of the global biogeochemical cycles we Berkeley, CA 94720, USA. Tonian, around 850 million years ago, observe today. E-mail: [email protected] but with little obvious impact to the Current Biology 25, R845–R875, October 5, 2015 ©2015 Elsevier Ltd All rights reserved R859 Current Biology Magazine Bilateria Rodinia Cnidaria Porifera Breakup δ13C Gaskiers Marinoan +5 0 Mesoproterozoic Palaeozoic -5 Sturtian giaciation ? Tonian Cryogenian Ediacaran Cambrian 1000 million years ago 750 635 541 Current Biology Figure 1. The Neoproterozoic. Diagram of the Neoproterozoic Era illustrating the large scale correlation between evolutionary innovation, climate perturbation, and trends in the 13C of marine carbonates (a refl ection of the global carbon cycle). Patterns in the distribution of protistan-grade fossils are depicted below the 13C curve and in- clude pre-Cryogenian ornamented microfossils (orange; typically asymmetrical, moderately large and stratigraphically long-lived), ‘vase-shaped’ microfossils (purple), scale microfossils (green), Ediacaran-age ornamented and ‘embryo’ microfossils (red; typically symmetrical and large, with ‘embryos’ sometimes occurring within the lumen of ornamented forms), Ediacaran macrofossils (grey), and ornamented Cambrian microfossils (dark orange; typically symmetrical and small). Bars above the 13C curve represent molecular clock estimates for the fi rst appearance of major metazoan groups (from Erwin et al. 2011), with white stars marking the fi rst ‘suggestive’ occurrence of corresponding fossils, and red stars indicating fi rst ‘convincing’ occurrence of such fossils. 13C data taken primarily from Halverson et al. (2010) and Lenton et al. (2014), with early Tonian data from Xiao S. et al. (2014) Biostratigraphic and chemostratigraphic constraints on the age of early Neoproterozoic carbonate successions in North China. Precambrian Res. 246, 208–225. Note that there are substantial dif- ferences of opinion over the stratigraphic correlation of much of the data depicted here, particularly with respect to the age-range of Ediacaran microfossils and the relationship between the Gaskiers glaciation and carbon isotope excursions. The boundary between the Tonian and the Cryogenian has yet to be formally defi ned. The dashed line at ~530 million years ago marks the onset of rapid evolutionary change, and regime shift into recognizably Phanerozoic style ecological and evolutionary dynamics, the ‘Cambrian Explosion’, as well as return to the relatively equable 13C expression of the early Tonian. The end of the Neoproterozoic Era (and Proterozoic Eon) is coincident with the beginning of the Palaeozoic Era (and Phanerozoic Eon). system beyond increased variability in ice-sheets repeatedly