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2009 Annual Science Report

Massachusetts Institute of Technology Reporting  |  JUL 2008 – AUG 2009

Executive Summary

Molecular and Fossil Records of Complex Life

During the reporting period, members of the MIT Team of the NAI have been investigating aspects of the molecular records of animal evolution. We do this through complementary studies of the genomes of modern taxa and the ancient organic molecules preserved in sedimentary rocks. In the Jacobs laboratory, studies of the jellyfish Aurelia are yielding greater understanding of the evolution of sensory and neural systems in the various life history stages of Cnidaria, the most basal branch of animals having well-established multimodal sensory systems and neural organization. Studies of Neanthes, a Polychaete worm, are yielding insights into the basal evolution of sensory organization in the Bilateria. These observations are shaping a better understanding of shared aspects of gene regulation of sensory organization in Cnidaria and Bilateria, and the discretely different modes of sensory organization and neural complexity found in these two groups. At the same time, members of the King laboratory are gaining new insights into the origin of animal multicellularity through their effort to reconstruct the genome of the last common ancestor of animals and their sister group, the choanoflagellates. While genome sequences of diverse animals are already available, only two choanoflagellates (Monosiga brevicollis and Proterospongia sp.) have been sequenced so far and they each show evidence of genome reduction and gene loss. Therefore, four species that represent choanoflagellate clades not previously sequenced, Salpingoeca napiformis, Salpingoeca urceolata, Diaphanoeca grandis, and Acanthoeca spectabilis are being processed. Also underway is a complementary study of the hedgehog signaling pathway. The hedgehog protein, a key regulator of developmental patterning in bilaterian animals, signals through the primary cilium which is equivalent to the choanoflagellate flagellum. We have identified core components of the hedgehog signaling pathway in M. brevicollis that were previously known only from animals. Interestingly, it was recently hypothesized that the hedgehog signaling pathway evolved from the hopane triterpenoid biosynthetic pathway in bacteria.

Collaboration between the Peterson and King laboratories has followed a unique approach to unravelling metazoan interrelationships by combining an analysis of microRNAs with traditional molecular phylogenetic approaches. Small non-coding RNA molecules, the microRNAs, regulate the translation of messenger RNAs and are a new and powerful tool to test competing hypotheses about animal relationships. An example that was tested this year is the phylogenetic position of the hexactinellid sponges relative to the demosponges. Using two independent approaches the Peterson group showed that demosponges are monophyletic, and that hexactinellids are the sister taxon of the demosponges (Silicea). Then, using a molecular clock, they estimated that hexactinellids diverged from demosponges over 700 Ma ago, and that the major radiation of demosponge taxa, including the spicule-bearing ones, all occurred well before the Cambrian. Thus the absence of siliceous spicules during the Ediacaran and Cryogenian cannot reflect the first appearance of the respective crown groups (contra Brocks & Butterfield, 2009), but instead reflects a massive failure to preserve siliceous spicules during the Precambrian (Sperling et al., 2009). All available data strongly suggest that demosponges are indeed the source of the sterane hydrocarbon biomarkers reported this year by Love and co-workers (Love et al., 2009) and based on research carried out in the Summons laboratory. Thus, multiple lines of evidence gathered by numerous members of the MIT team are suggesting that metazoan multicellularity has its roots in the Cryogenian (see Figure 1).

In respect to paleontological findings about the origin of animals, we have been developing a new database of Ediacaran-Cambrian fossil occurrences for use in a study of the role of ecosystem engineering. We have also made major inroads into improved precision for dating Neoproterozoic events via the U-Pb isotope system. Progress has also been made on quantitative models of this process (Krakauer et al. 2009) and in the role of hierarchical structuring of developmental regulatory systems (Erwin & Davidson 2009). Further, and in regard to the evolution of plants, members of the Knoll Laboratory have investigated the hydraulic consequences of anatomical development in early land plants. They adapted a model of water transport in xylem cells that accounts for resistance to flow from the lumen, pits, and pit membranes, and that can be used to compare extinct and extant plants in a quantitative way. Application of this model to early vascular plants indicates that extinct seed plants evolved a structural and functional diversity of xylem architectures broader, in some ways, than the range observable in living seed plants.

Metabolism and Environmental Redox

Metabolic networks perform some of the most fundamental functions in living cells, including energy transduction and building block biosynthesis. While these are the best characterized networks in living systems, understanding their evolutionary history and complex wiring is still a major open question in biology. In order to understand the evolution and dynamics of metabolism in microbial ecosystems, members of the Segre group have extended their genome-scale flux balance models of metabolism to multiple interacting species. They did this by analogy to compartmentalization in the well characterized metabolic model of the yeast Saccharomyces cerevisiae, which we treated as an “ecosystem of organelles”. They have also evaluated the arithmetic simplicity beneath metabolic network architecture. Models of the behaviors of metabolic pathways display a modular organization of recurring topologies, including autocatalytic cycles, and a logarithmic dependence of pathway length on input/output molecule size. Similar properties hold for real metabolic networks, suggesting that optimality principles and arithmetic simplicity underlie biochemical complexity.

A paper from Harvard members, Johnston et al. (2009), illustrates how contributions to primary production by anoxygenic photoautotrophs may have influenced biogeochemical cycling during the Proterozoic. The ability to generate organic matter (OM) using sulfide as an electron donor enabled a positive biogeochemical feedback that sustained mid-water euxinia (H2S). On a geologic time scale, pyrite precipitation and burial governed a second feedback that moderated H2S availability and water column oxygenation. This limited the accumulation of O2 in the atmosphere and ocean. Thus, the breaking of this feedback loop precipitated Earth’s transition from its prokaryote-dominated middle age, removing a physiological barrier to eukaryotic diversification (ie hydrogen sulfide which is toxic to all eukryotes) and, ultimately, the evolution of complex multicellular organisms. Aspects of this new hypothesis are now being studied via a modern analogue beneath Taylor Glacier, an outlet glacier of the East Antarctic Ice Sheet (Mikucki et al., 2009). Related to the Neoproterozoic-Cambrian redox transition is the possibility that the late Proterozoic oceans were rich in dissolved organic carbon (DOC). To understand how such a DOC buildup could be possible, Rothman’s group is studying the dependence of the DOC reservoir on respiration rates. In their recent studies of well controlled systems, respiration rates are found to be widely distributed in a predictable way, and the size of the DOC reservoir has been related to this distribution. Theoretical predictions suggest that small changes in the slowest rates, as one might expect during transitions between anoxic and oxic environments, lead to large changes in the size of the DOC reservoir along with concomitant large fluctuations in the isotopic record. In related work, Rothman’s group has also provided theoretical constraints on the duration and mechanism of the Shuram-Wonoka-Doushantuo carbon-isotopic excursion. Going forward, we plan to test the hypothesis that prolific anoxygenic photosynthesis was modulating the oxygen content of the Proterozoic ocean by looking at the diversity of cyanobacteria that are able to use sulfide as an electron donor for photosynthesis.

Mars Exploration

NASA spacecraft have discovered both chemical and physical evidence that liquid water once flowed on the martian surface. Close examination of the images and spectroscopic data from these spacecraft, and understanding what they tell us, are critical to selecting the best sites for future rover missions. Our Astrobiological Exploration of Mars project aims to maximise the knowledge gained from orbiting and landed spacecraft and apply it effectively in future planning and execution of new missions. The key questions for astrobiology are no longer “was water present?” rather “what were its properties?” and “How long did it persist?” Using thermodynamic calculations, one can approach both questions, using mineral identifications made by the MER rovers and CRISM. We find that waters at Gusev and Meridiani planum grew extremely salty as evaporation proceeded, reaching conditions that would challenge known life on Earth. We also learn that in a number of places on the martian surface, minerals deposited billions of years ago as a result of water-rock interactions have seen little or no water since that time. In an effort to put this new knowledge to practical use, Knoll and Summons currently participate in the MSL Biosignature/Carbon Compound Preservation Working group (Summons is Chair) that was chartered by the MSL Project and NASA HQ. The core objective of the MSL mission is the elucidation of both early Martian surface environments, particularly those which may have been habitable by microorganisms, and early Martian surface processes, particularly those which may have been favorable for the preservation of microbial biosignatures and/or abiotic organic compounds. The pursuit of this goal is what will distinguish MSL from all previous missions, and it provides a well-defined pathway for the focus of landed surface operations. The objective of the Biosignature/Carbon Compound Preservation Working group is to assess the potential diversity of “taphonomic windows” that may be recorded in the ancient terrains that MSL will be exploring. The synergy between the search for taphonomic windows on the MSL mission and our NAI research which in part explores how organisms and other biosignatures become preserved in Earth’s early rock record is clear.

Extrasolar Planets

Lisa Kaltenegger and Dimitar Sasselov worked on the detection of terrestrial planets with alternative geochemical cycles, for example, atmospheres with enhanced concentrations of SO2 that are detectable via future NASA space missions. Lisa and Dimitar also developed models of detectable features of water dominated super-Earths and conducted an associated outreach activity through interviews on the History Channel and the Discovery Channel. In collaboration with UK microbiologists Cockell and Raven they published new models for remotely detectable features of planetary environments that are dominated by cryptic photosynthesis.

Education and Public Outreach

The team’s website, incorporating a method of communicating the activities of the MIT group with the general public and a method of intra-team communications was developed and launched this year. We aim to develop this as a focal point for education and research into all aspects of the Ediacaran biota and also as an “Encyclopedia of Early Complex Life”. Images will form some of the content, as well as descriptions, taxonomy and references coming from existing materials from within the team. As a second step, we held a field excursion to the Mistaken Point area of Newfoundland which is the fossil site of the earliest known complex life on Earth. Peter Mangiafico used publicly available software to create zoomable and panable images taken on the field excursion. Two of these photosynths are found on the journal page. Photosynth is a technology similar to Gigapan that allows for many photographs to be stitched together in a way that is easily zoomable and panable in a web browser. A large amount of video and still images of the trip have been gathered together for the purpose of developing a virtual field trip for a lay audience.

Bowring has developed a program to teach the science of geochronology to high school students. With roots in the NSF funded EARTHTIME project, it has since grown rapidly with the aim of teaching the details of radioactive decay, isotope dilution and their application of dating volcanic ash beds interlayered with fossil bearing rocks to understanding earth history. Modules will show how geochronology can be used to constrain the early evolution of animals as well as the age an duration of global, Snowball, glaciations that introduce uncertainties in geochronology and stratigraphic sequence. The activities can be taught both at MIT and as part of a mobile lab. At the same time, the Summons laboratory is developing a paleontology module for teaching evolutionary concepts. This will be initially trialed at middle schools in the outer Boston area. Independently, Lisa Kaltenegger contributed to several summer schools concerned with astronomy and detection of extrasolar planets.

Lastly, and most importantly for mission-related science, John Grotzinger has been leading an effort to educate the wider scientific community about the capabilities and complexity of the forthcoming Mars Science Laboratory mission as well as bringing the community of diverse MSL stakeholders together. He is endeavoring to focus attention on this mission as a quest for habitable environments, particularly those that might have preserved biosignatures had they been present. The challenges facing MSL far exceed those encountered in building and flying the MER Rovers. The complexity of the payload means that the leadership and execution of the landed operations will require unprecedented cooperation between the science and engineering teams and a large body of expert collaborators.