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2014 Annual Science Report

Massachusetts Institute of Technology Reporting  |  SEP 2013 – DEC 2014

Executive Summary

THEME I: THE EARLIEST HISTORY OF ANIMALS

Members of the MIT Team have been working on some of the oldest chemical and body fossil evidence of animals, and applying studies of genomes and modern animal development to interpret these fossils. The goal is to understand how the interactions between changes in the physical environment, ecological interactions and in developmental mechanisms in evolutionary innovations lead to greater biological complexity.

Post-doctoral fellow David Gold has been investigating the origins and biosynthesis of a steroidal hydrocarbon proposed as a biomarker for sponges, the earliest-branching animals. This molecular record of sponges extends to the Cryogenian period. He has been studying both the distribution of this compound—24-isopropylcholestane—in samples of living and fossil sponges, and the distribution of the genes required for its synthesis in genomes across extant eukaryotes. The results support the conclusion that this compound is a true sponge biomarker. Pelagophyte algae, proposed by some as an alternative source, arose later in the Phanerozoic.

The size of early multicellular organisms was sufficient to modify their local environment. Work led by members of the Jacobs lab modeled Neoproterozoic frond-like forms in the earliest-known communities of multicellular organisms and demonstrated that they were of sufficient scale and density to generate a distinctive canopy flow-regime. This process yielded a selective advantage towards the larger forms that evolved at this time. This result is a function of limits imposed by diffusion at the surface of organisms, and how height and attendant velocity exposure are a means to escape these limits. Building on these results, they are now developing additional models of abiotic/biotic interactions at the surfaces of living organisms. Ultimately, this work will help illuminate how animals, initially dependent on passive diffusion, developed more complex feeding behaviors.

Understanding the evolution of integrated sensory organs—such as the eyes, ears and nose that develop in concert on our heads—is fundamental to understanding animal complexity. These are the features that permit movement and the environmental responses that characterize animals. Other work in the Jacobs lab examined poorly studied early branches of the animal family tree, with a focus on the jellyfish Aurelia. Their aim was to learn how the genetic regulation of sensory organs is conserved in some cases and evolves in others. Comparison of developmental regulation reveals how similar gene networks can be differentially modified and deployed, permitting the evolution of complex sensory systems. Jellyfish provide an ideal study system for the examination of the evolution of such sensory systems in animal evolution, as they are the most basal branch in the animal tree with multiple sensory modes, and these develop at multiple stages in a complex life history. This provides us the ability to compare and contrast within the broader cnidarian group to which jellyfish belong, and to the bilaterians, the broad group containing humans and most other animals. The application of genomic methods greatly enhances our ability to pursue these questions.

Research in the Knoll lab has focused on three major issues relevant to early animal evolution. First, Knoll and colleagues developed a hypothesis to explain the mid-Neoproterozoic diversification of eukaryotes by invoking the evolution of eukaryote-eating protists (analogous to the evolution of carnivores driving the Cambrian diversification of animals). Second, work to integrate ecological data from modern oxygen-minimum zones with paleontological and geochemical data has yielded insights on early animal evolution. Finally, collaborations with other groups have focused on a variety of topics including the preservation of tiny animals in phosphate in the earliest Cambrian, a new Neoproterozoic record of vase-shaped protists.

We have also been carrying out a number of studies in support of our objective to investigate the controls on the preservation of the geologic record of complex life on earth, with the ultimate aim of allowing the fossil evidence for the succession of events to be constrained and interpreted. In the Briggs lab, these studies include investigating the connections between taphonomy and ecology of the Ediacara Biota based on the collection of fossil specimens and their careful examination, laboratory experiments designed to better understand how these fossils became preserved in different settings, and investigations of how Proterozoic eukaryotic microfossils are preserved, again from studying both new fossil material through a variety of approaches, and performing analog experiments in the laboratory.

The Peterson lab has continued its focus on micro-RNAs (miRNA) in order to better understand the relationship between genetic and phenotypic diversity. Toward this goal, they have established a new database of miRNA genes (as opposed to sequences) assembled under strict quality control and an entirely novel nomenclature, bridging the different names previously given to the same gene across taxa. This database allows the evolution of miRNA genes to be studied across the animal kingdom. Such study shows that miRNA evolution is not correlated to the duplication of genetic material, but shaped by periods of intense miRNA innovation.

The focus of the Erwin group remained on the origins of novelty and innovation, particularly associated with the origin and early diversification of animals during the Cryogenian, Ediacaran and early Cambrian. A field campaign in Namibia yielded new specimens, new fossil localities, and a potential new organism from the Ediacaran. Work on the phylogeny of early Cambrian lobopods was carried out to test the hypothesis that arthropods evolved from this enigmatic group of organisms.

The biomarker approach we typically apply to study the earliest animals and their evolutionary environments has application to more recent contexts such as providing direct palaeodietary information on early humans. In a study conducted with collaborators in Spain, we showed that Neanderthals had a high rate of conversion of cholesterol to coprostanol related to the presence of specific types of bacteria in their guts. Analysis of sterols from five sediment samples, containing human coprolites, from different occupation floors of the El Salt cave site in Spain indicate that Neanderthals predominantly consumed meat.

THEME II: PALEONTOLOGICAL, SEDIMENTOLOGICAL AND GEOCHEMICAL INVESTIGATIONS OF THE MESOPROTEROZOIC-NEOPROTEROZOIC TRANSITION

As we learn more about the earliest evolutionary history of animals and other complex multicellular organisms, it becomes clearer that a satisfactory understanding of these events must be set within the broader context of late Mesoproterozoic and early Neoproterozoic biological and environmental change. To this end, several labs within our team have directed considerable energy to document and understand Mesoproterozoic and Neoproterozoic sedimentary successions. Over the reporting period, this has included stratigraphic and sedimentological fieldwork on rocks of this age in northwestern Canada, Death Valley, Mongolia, and anaylsis of drill cores from Russia, Congo and Zambia. Progress has also been made in new techniques for the discovery and description of Proterozoic microfossils and the processes forming such sedimentary phenomena as ooids and wrinkle structures. We have made several fold improvements in the precision of oxygen-17 measurements, which can record the balance of atmospheric oxygen and carbon dioxide, and in measurements of nitrogen isotopes in ancient pigments, a potential redox tracer for the Proterozoic.

The Summons lab has been researching a range of molecular and isotopic phenomena aimed at shedding light on what controls Neoproterozoic ocean redox, evolutionary trends in the abundances of molecular fossils (biomarkers) and the enigmatic natural variability carbon isotopic compositions of organic and inorganic carbon at this time. Our studies of carotenoid pigment biomarkers for green and purple sulfur bacteria have revealed that they are ubiquitous in rock extracts of Proterozoic to Paleozoic age—implying that the shallow oceans became sulfidic more frequently than previously thought. Other projects focused on the biosynthesis of another important biomarker, the hopanoids, vesicles released from marine bacteria for interaction between cells and their environment, and the molecular signatures of microbial communities in hot springs in Yellowstone National Park.

THEME III: THE NEOPROTEROZOIC CARBON CYCLE

Both the rise of complex life in the Neoproterozoic and the Phanerozoic mass extinctions are accompanied by significant perturbations of the carbon cycle. The attention of most research to date has been focused on causality and environmental change has almost always almost been considered the driver. Yet the co-evolution of life and the environment suggests that the fundamental issue is not causality but rather stability. Current research in the Rothman lab seeks to develop a theory of biosphere-geosphere stability and to test it using the geochemical and fossil records.

THEME IV: TAPHONOMY, CURIOSITY AND MISSIONS TO MARS
Members of our team continue to be involved in both the MER and MSL missions on Mars. On the latter mission, team members have recently documented a long-lived, habitable environment in Gale Crater dominated by rivers and lakes. Research on the mineralogy and geochemistry of rocks at the base of Mt Sharp has improved our understanding of their complex diagenetic history. Progress has also been made in linking orbital observations with those made by the rovers; this has been advanced particularly by field research at Rio Tinto and detailed laboratory experiments that constrain the relationship between mineral combinations and their signatures in infrared reflectance spectroscopy—and their effect on our ability to detect organics.

Summons was co-chair of the Organic Contamination Panel, commissioned by Michael Meyer and Lisa May of NASA HQ, that comprehensively examined issues pertaining to organic contamination, and its management, for the Mars2020 rover mission.

THEME V: REVIEW AND SYNTHESIS
We produced several review articles on aspects of biomarker formation and preservation. One was aimed at a general audience and the other was specifically prepared for a paleontology short course and to illustrate how molecular records can provide useful information about environments in which organisms thrived.

Publications

  • Aponte, J. C., Tarozo, R., Alexandre, M. R., Alexander, C. M. O. D., Charnley, S. B., Hallmann, C., … Huang, Y. (2014). Chirality of meteoritic free and IOM-derived monocarboxylic acids and implications for prebiotic organic synthesis. Geochimica et Cosmochimica Acta, 131, 1–12. doi:10.1016/j.gca.2014.01.035

  • Arvidson, R. E., Squyres, S. W., Bell, J. F., Catalano, J. G., Clark, B. C., Crumpler, L. S., … Wolff, M. J. (2014). Ancient Aqueous Environments at Endeavour Crater, Mars. Science, 343(6169), 1248097–1248097. doi:10.1126/science.1248097

  • Biller, S. J., Schubotz, F., Roggensack, S. E., Thompson, A. W., Summons, R. E., & Chisholm, S. W. (2014). Bacterial Vesicles in Marine Ecosystems. Science, 343(6167), 183–186. doi:10.1126/science.1243457

  • Blaney, D. L., Wiens, R. C., Maurice, S., Clegg, S. M., Anderson, R. B., Kah, L. C., … Madsen, M. B. (2014). Chemistry and texture of the rocks at Rocknest, Gale Crater: Evidence for sedimentary origin and diagenetic alteration. Journal of Geophysical Research: Planets, 119(9), 2109–2131. doi:10.1002/2013je004590

  • Bovee, R. J., & Pearson, A. (2014). Strong influence of the littoral zone on sedimentary lipid biomarkers in a meromictic lake. Geobiology, 12(6), 529–541. doi:10.1111/gbi.12099

  • Briggs, D. E. G. (2014). Paleontology: A New Burgess Shale Fauna. Current Biology, 24(10), R398–R400. doi:10.1016/j.cub.2014.04.010

  • Briggs, D. E. G., & Summons, R. E. (2014). Ancient biomolecules: Their origins, fossilization, and role in revealing the history of life. BioEssays, 36(5), 482–490. doi:10.1002/bies.201400010

  • Cabrol, N. A., Herkenhoff, K., Knoll, A. H., Farmer, J., Arvidson, R., Grin, E., … Aileen Yingst, R. (2014). Sands at Gusev Crater, Mars. Journal of Geophysical Research: Planets, 119(5), 941–967. doi:10.1002/2013je004535

  • Cady, L. P., Brack, A., Bueno Prieto, J. E., Cockell, C., Horneck, G., Kasting, J. F., … Pérez-Mercader, J. (2014). Where Do We Go from Here? Astrobiology Editorial Board Opinions. Astrobiology, 14(8), 629–644. doi:10.1089/ast.2014.1405

  • Creveling, J. R., Johnston, D. T., Poulton, S. W., Kotrc, B., Marz, C., Schrag, D. P., & Knoll, A. H. (2013). Phosphorus sources for phosphatic Cambrian carbonates. Geological Society of America Bulletin, 126(1-2), 145–163. doi:10.1130/b30819.1

  • Creveling, J. R., Knoll, A. H., & Johnston, D. T. (2014). TAPHONOMY OF CAMBRIAN PHOSPHATIC SMALL SHELLY FOSSILS. PALAIOS, 29(6), 295–308. doi:10.2110/palo.2014.002

  • Erwin, D. H. (2014). Temporal acuity and the rate and dynamics of mass extinctions: Fig. 1.. Proc Natl Acad Sci USA, 111(9), 3203–3204. doi:10.1073/pnas.1400431111

  • Erwin, D. H. (n.d.). Evolutionary Innovation. Oxford Bibliographies Online Datasets. doi:10.1093/obo/9780199941728-0060

  • Farley, K. A., Malespin, C., Mahaffy, P., Grotzinger, J. P., Vasconcelos, P. M., Milliken, R. E., … Moores, J. E. (2013). In Situ Radiometric and Exposure Age Dating of the Martian Surface. Science, 343(6169), 1247166–1247166. doi:10.1126/science.1247166

  • Field, D. J., Gauthier, J. A., King, B. L., Pisani, D., Lyson, T. R., & Peterson, K. J. (2014). Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles. Evolution & Development, 16(4), 189–196. doi:10.1111/ede.12081

  • French, K. L., Rocher, D., Zumberge, J. E., & Summons, R. E. (2015). Assessing the distribution of sedimentary C 40 carotenoids through time. Geobiology, 13(2), 139–151. doi:10.1111/gbi.12126

  • French, K. L., Sepúlveda, J., Trabucho-Alexandre, J., Gröcke, D. R., & Summons, R. E. (2014). Organic geochemistry of the early Toarcian oceanic anoxic event in Hawsker Bottoms, Yorkshire, England. Earth and Planetary Science Letters, 390, 116–127. doi:10.1016/j.epsl.2013.12.033

  • Ghisalberti, M., Gold, D. A., Laflamme, M., Clapham, M. E., Narbonne, G. M., Summons, R. E., … Jacobs, D. K. (2014). Canopy Flow Analysis Reveals the Advantage of Size in the Oldest Communities of Multicellular Eukaryotes. Current Biology, 24(3), 305–309. doi:10.1016/j.cub.2013.12.017

  • Gold, D. A., Gates, R. D., & Jacobs, D. K. (2014). The Early Expansion and Evolutionary Dynamics of POU Class Genes. Molecular Biology and Evolution, 31(12), 3136–3147. doi:10.1093/molbev/msu243

  • Hamilton, T. L., Bovee, R. J., Thiel, V., Sattin, S. R., Mohr, W., Schaperdoth, I., … MacAlady, J. L. (2014). Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake. Geobiology, 12(5), 451–468. doi:10.1111/gbi.12092

  • Hartenstein, V., & Jacobs, D. (2013). Developmental Plasticity, Straight from the Worm’s Mouth. Cell, 155(4), 742–743. doi:10.1016/j.cell.2013.10.038

  • Knoll, A. H. (2014). Paleobiological Perspectives on Early Eukaryotic Evolution. Cold Spring Harbor Perspectives in Biology, 6(1), a016121–a016121. doi:10.1101/cshperspect.a016121

  • Knoll, A. H., & Sperling, E. A. (2014). Oxygen and animals in Earth history. Proceedings of the National Academy of Sciences, 111(11), 3907–3908. doi:10.1073/pnas.1401745111

  • Lanza, N. L., Fischer, W. W., Wiens, R. C., Grotzinger, J., Ollila, A. M., Cousin, A., … Sautter, V. (2014). High manganese concentrations in rocks at Gale crater, Mars. Geophysical Research Letters, 41(16), 5755–5763. doi:10.1002/2014gl060329

  • Mariotti, G., Perron, J. T., & Bosak, T. (2014). Feedbacks between flow, sediment motion and microbial growth on sand bars initiate and shape elongated stromatolite mounds. Earth and Planetary Science Letters, 397, 93–100. doi:10.1016/j.epsl.2014.04.036

  • Mariotti, G., Pruss, S. B., Perron, J. T., & Bosak, T. (2014). Microbial shaping of sedimentary wrinkle structures. Nature Geosci, 7(10), 736–740. doi:10.1038/ngeo2229

  • McAdam, A. C., Franz, H. B., Sutter, B., Archer, P. D., Freissinet, C., Eigenbrode, J. L., … Wray, J. J. (2014). Sulfur-bearing phases detected by evolved gas analysis of the Rocknest aeolian deposit, Gale Crater, Mars. Journal of Geophysical Research: Planets, 119(2), 373–393. doi:10.1002/2013je004518

  • Nachon, M., Clegg, S. M., Mangold, N., Schröder, S., Kah, L. C., Dromart, G., … Wellington, D. (2014). Calcium sulfate veins characterized by ChemCam/Curiosity at Gale crater, Mars. Journal of Geophysical Research: Planets, 119(9), 1991–2016. doi:10.1002/2013je004588

  • Ono, S., Sim, M. S., & Bosak, T. (2014). Predictive isotope model connects microbes in culture and nature. Proc Natl Acad Sci USA, 111(51), 18102–18103. doi:10.1073/pnas.1420670111

  • Palucis, M. C., Dietrich, W. E., Hayes, A. G., Williams, R. M. E., Gupta, S., Mangold, N., … Sumner, D. Y. (2014). The origin and evolution of the Peace Vallis fan system that drains to the Curiosity landing area, Gale Crater, Mars. Journal of Geophysical Research: Planets, 119(4), 705–728. doi:10.1002/2013je004583

  • Pearson, A. (2014). Lipidomics for Geochemistry. Treatise on Geochemistry, None, 291–336. doi:10.1016/b978-0-08-095975-7.01022-6

  • Rooney, A. D., MacDonald, F. A., Strauss, J. V., Dudas, F. O., Hallmann, C., & Selby, D. (2013). Re-Os geochronology and coupled Os-Sr isotope constraints on the Sturtian snowball Earth. Proceedings of the National Academy of Sciences, 111(1), 51–56. doi:10.1073/pnas.1317266110

  • Rothman, D. H. (2014). Earth’s carbon cycle: A mathematical perspective. Bulletin of the American Mathematical Society, 52(1), 47–64. doi:10.1090/s0273-0979-2014-01471-5

  • Rothman, D. H., Fournier, G. P., French, K. L., Alm, E. J., Boyle, E. A., Cao, C., & Summons, R. E. (2014). Methanogenic burst in the end-Permian carbon cycle. Proceedings of the National Academy of Sciences, 111(15), 5462–5467. doi:10.1073/pnas.1318106111

  • Schmerk, C. L., Welander, P. V., Hamad, M. A., Bain, K. L., Bernards, M. A., Summons, R. E., & Valvano, M. A. (2014). Elucidation of the B urkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria. Environmental Microbiology, 17(3), 735–750. doi:10.1111/1462-2920.12509

  • Schubotz, F., Hays, L. E., Meyer-Dombard, D. A. R., Gillespie, A., Shock, E. L., & Summons, R. E. (2015). Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.00042

  • Siebach, K. L., Grotzinger, J. P., Kah, L. C., Stack, K. M., Malin, M., Léveillé, R., & Sumner, D. Y. (2014). Subaqueous shrinkage cracks in the Sheepbed mudstone: Implications for early fluid diagenesis, Gale crater, Mars. Journal of Geophysical Research: Planets, 119(7), 1597–1613. doi:10.1002/2014je004623

  • Sistiaga, A., Mallol, C., Galván, B., & Summons, R. E. (2014). The Neanderthal Meal: A New Perspective Using Faecal Biomarkers. PLoS ONE, 9(6), e101045. doi:10.1371/journal.pone.0101045

  • Sperling, E. A., Rooney, A. D., Hays, L., Sergeev, V. N., Vorob’eva, N. G., Sergeeva, N. D., … Knoll, A. H. (2014). Redox heterogeneity of subsurface waters in the Mesoproterozoic ocean. Geobiology, 12(5), 373–386. doi:10.1111/gbi.12091

  • Stack, K. M., Grotzinger, J. P., Kah, L. C., Schmidt, M. E., Mangold, N., Edgett, K. S., … Wiens, R. C. (2014). Diagenetic origin of nodules in the Sheepbed member, Yellowknife Bay formation, Gale crater, Mars. Journal of Geophysical Research: Planets, 119(7), 1637–1664. doi:10.1002/2014je004617

  • Strauss, J. V., Rooney, A. D., MacDonald, F. A., Brandon, A. D., & Knoll, A. H. (2014). 740 Ma vase-shaped microfossils from Yukon, Canada: Implications for Neoproterozoic chronology and biostratigraphy. Geology, 42(8), 659–662. doi:10.1130/g35736.1

  • Summons, R. E., Sessions, A. L., Allwood, A. C., Barton, H. A., Beaty, D. W., Blakkolb, B., … Steele, A. (2014). Planning Considerations Related to the Organic Contamination of Martian Samples and Implications for the Mars 2020 Rover. Astrobiology, 14(12), 969–1027. doi:10.1089/ast.2014.1244

  • Tarhan, L. G., & Droser, M. L. (2014). Widespread delayed mixing in early to middle Cambrian marine shelfal settings. Palaeogeography, Palaeoclimatology, Palaeoecology, 399, 310–322. doi:10.1016/j.palaeo.2014.01.024

  • Tarhan, L. G., Droser, M. L., Gehling, J. G., & Dzaugis, M. P. (2015). Taphonomy and morphology of the Ediacara form genus Aspidella. Precambrian Research, 257, 124–136. doi:10.1016/j.precamres.2014.11.026

  • Tarhan, L. G., Hughes, N. C., Myrow, P. M., Bhargava, O. N., Ahluwalia, A. D., & Kudryavtsev, A. B. (2013). Precambrian-Cambrian boundary interval occurrence and form of the enigmatic tubular body fossil Shaanxilithes ningqiangensis from the Lesser Himalaya of India. Palaeontology, 57(2), 283–298. doi:10.1111/pala.12066