Summary: How can matter transition from the nonliving to the living state? The answer is essential for understanding the origin of life on Earth and for identifying promising targets in the search for life on other planets. Most studies have focused on the likely chemistry of RNA (1), protein (2), lipid, or metabolic “worlds” (3) and autocatalytic sets (4), including attempts to make life in the lab. But these efforts may be too narrowly focused on the biochemistry of life as we know it today. A radical rethink is necessary, one that explores not just plausible chemical scenarios but also new physical processes and driving forces. Such investigations could lead to a physical understanding not only of the origin of life but also of life itself, as well as to new tools for designing artificial biology

Cronin, Leroy

Walker, Sara Imari

English

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Beyond prebiotic chemistry

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           Cronin, L., and Walker, S. I. (2016) Beyond prebiotic chemistry.  Science, 352(6290), pp. 1174-1175.      © 2016 AAAS      This is the author peer reviewed version of the above article, which has been published in final form at DOI: 10.1126/science.aaf6310   Please cite only the published version using the reference above.                   http://eprints.gla.ac.uk/122685/       Deposited on: 12 August 2016      Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk Beyond prebiotic chemistry What dynamic network properties allow the emergence of life? By Leroy  Cronin1  and  Sara  Imari  Walker2     How  can  matter  transition from  the  non-living to  the  living  state?  The  answer  is essential for understanding the origins of life on Earth  and for identifying promising targets in the search  for life on other planets. Most studies have focused on the likely chemistry of RNA (1), protein (2), lipid, or metabolic “worlds” (3) and autocatalytic sets  (4),  including attempts to make  life  in the  lab.  But  these  efforts may  be too narrowly focused on the biochemistry of life  as we know  it today.  A radical re-think is necessary—one that  goes  beyond  investigations into  plausible chemical scenarios to explore not just new chemistries, but also new physical processes and driving forces. Such  investigations could  lead  to a physical understanding not only  of the origin  of life but also of life itself, as well as to new tools  for designing artificial biology.  A transition from the limited function and memory possible in a soup of weakly interacting molecules to more strongly interacting networks was essential for the emergence of life on Earth. Left unattended, chemistry becomes more dilute and disordered. A route to complexity and enrichment that could lead to the development of evolvable units seems to be required quickly to avoid this serious issue. Yet, most research efforts have focused on detailing precise chemical mechanisms  for producing  high yields of individual  bio-inspired  products,  without  addressing  the  processes  necessary to form increasingly complex molecules and networks. What happens to our traditional perspectives if we do not restrict attention to the chemical substrates of known life? The development of  networks over time may be  more important than the specific chemical  nature  of  their  molecular components.  Even RNA can form cooperative  networks,  diversifying  its potential  role in the earliest evolving chemistries (7). Autocatalytic networks can evolve in the absence of genes (4), but much more work needs to be done to understand the messier heredity of chemical systems. The first networks would have had to be simple, challenging  the notion that highly complex and improbable  molecules  are needed to jump-start  life. The molecular  constituents  of simple networks are more likely to arise by chance than the highly evolved molecules of extant life. Starting from networks composed of simple molecules could therefore dramatically  reduce the time necessary for the emergence of life, and potentially increase the probability of an origins event, A concept of information  relevant to biological organization  may be essential to identifying these networked processes. Adami and LaBar have described life at a basic level as “information that copies itself” (8). Given that life not only copies information  but also uses information  to construct itself, we might instead describe the start of life as “simple machines that can construct slightly more complicated  machines.” Focusing on information moves the narrative even further away from a chemistry-specific model than focusing on networks alone, but may perhaps provide our best shot at uncovering universal “laws of life” that work not just for biology of known chemistry, but also for putative artificial and alien life. For example, information-theoretic measures have recently been shown to distinguish biological networks from random, even in cases where the biological networks share important network properties with random networks, such as common topological features (9). Life requires chemistry, but it is the dynamical properties of that chemistry—including both the temporal and spatial organization of molecular networks and their information management—from which the properties of the living state emerge. Another  way  to reconceptualize the  problem  is to  consider  life’s  emergence  as a phase  transition  in  the  origin  of the  biosphere  as  a  whole.  This  phase  transition   manifests  as  a  sudden  change  in  the  way  that  chemistry  is able  to process   and  use  information   and  to  utiliz e   fr e e   e ne r g y .  It  requires   new  approaches   to  understanding  how  the organization of energy flows can lead to the emergence of increasingly complex networks over time (6). Heterogeneity in the early  Earth  environment  played  a very important  role in facilitating  the emergence  of life by helping  to sustain,  select, and  drive  the  emergence  of  organized  systems  that  could  persist  over  time.  For  example,  pores  in  rocks  may  have influenced chemical selection, leading to increasingly life-like chemistries over time (10).   One important order parameter in characterizing life’s origin as a phase transition is the homochirality. Jafarpour et al. have shown that homochirality  emerges spontaneously as a symmetry-breaking process in mo d e l s o f noisy autocatalytic systems,  a result that could be experimentally tested (5). Insights  may also come from studying  other transitions  in the biosphere   where  organization   has  emerged  from  messy  dynamical   systems,   including   the  origins  of  social  systems (11). Such comparisons could yield insights into universal properties of dynamic networks. However,    speculation    should    be   restricted    to   the   development    of   experimentally   testable   hypotheses   that address key questions and provide a focus for progress. First, how did evolution begin if the machinery  for evolution was not in place? Experimental studies addressing this question could evaluate the evolvability  and robustness  in molecular networks or systems with a lower molecular complexity than a full-blown ribosome. Second, can the emergence of life be substrate-independent? Answers  may come from investigation  of evolvable  chemical  pathways  in the laboratory  that are                                                                                        based on alternative polymers. This includes demonstrating how function  *WestCHEM,  School   of  Chemistry, University of Glasgow, Glasgow G12  8QQ (UK);  Email:  Lee.Cronin@glasgow.ac.uk †School of Earth  and  Space  Exploration and   Beyond    Center    for   Fundamental Concepts  in   Science,  Arizona  State University,  Tempe   AZ   USA   and   Blue Marble   Space   Institute  for  Science, Seattle      WA        USA;        Email: sara.i.walker@asu.edu can  be  transferred  between  molecules  with  different  chemical  make-up while preserving the overall network structure. Third, at what point in the historical  origins  of  life  did  the  current  chemistry  of  life  get  selected? Could  more than one version  of biology  exist  on Earth  today  or in the past? This could in principle be tested in one-pot experiments that include in-vitro competition between alternative chemical scenarios for early life. t In more abstract terms, it remains unclear whether life’s origin, evolution, and understanding the living state will be understood within a common conceptual paradigm, or will be shown to involve different processes (12, 13). Here, practical issues become important in connecting these areas. For example, how complex must a chemical signature need to be before it can be considered  a biosignature? Looking  for complex  objects  that could  not form randomly  in an environment, but arise only as a result of life-like machinery, might help in classifying potential biosignatures and the processes that generate them. Earth’s complex inorganic and organic worlds are certainly highly connected in this respect, with even Earth’s mineral diversity in part dictated by life (14). Progress  will  be made  by challenging  all historical  prerequisites  assumed  to  be  important  in the  origin  of life.  We should be considering measurable routes to developing new physics and chemistry to understand life’s origins and the living state. Not only is a new understanding of what it means for a physical system to be ‘alive’ possible, but a new multinational project to search for new life on Earth (15), generate new life in the lab or in silico, and to explore the potential for new life on other worlds (16), can potentially be connected in deep and novel ways.  What is needed is for researchers to challenge our own dogmas and intrinsic bias, and be willing to work across boundaries to construct a new model for the living state,, inspiring an era of ‘big science’ focused on origins and the development of new life forms resulting from theory-driven experiments.   REFERENCES 1. S. A. Benner, H. J. Kim, M. A. Carrigan, Acc. Chem. Res. 45, 2025 (2012). 2. M. Rodriguez-Garcia et al., Nat. Commun. 6, 8385 (2015) 3. J. C. Blain, J. W. Szostak, Ann. Rev. Biochem., 83, 615 (2014). 4. V. Vasas, C. Fernando, M. Santos, S. A. Kauffman, E. Szathmary, Biology Direct, 7, 1 (2012). 5. F. Jafarpour, T. Biancalani, N. Goldenfeld, Phys. Rev. Lett. 115, 158101 (2015). 6. H. Morowitz, E. Smith. Complexity 13. 51 (2007). 7. N. Vaidya et al. Nature 491, 72 (2012). 8. C. Adami, T. LaBar, From Entropy to Information: Biased Typewriters and the Origin of Life, see http://arxiv.org/abs/1506.06988. 9. S. I. Walker, H. Kim, P. C. W. Davies, Phil. Trans. R. Soc. A 374, 20150057 (2016). 10. W. Martin, M. J. Russell, Phil. Trans. R. Soc. Lond. B, 358, 59 (2003). 11. S.DeDeo, Major Transitions in Political Order, see http://arxiv.org/abs/1512.03419. 12. D. H. Erwin, Curr. Biol. 25, R930 (2015). 13. E. Bapteste, Trends Genet. 29, 439 (2013). 14. E. G. Grosch, R. M. Hazen, Astrobiology 15, ast.2015.1302 (2015). 15. P. C. W. Davies, Philos. Trans. R. Soc. A 369, 624 (2011). 16. S. Seager, W. Bains, Sci. Adv. 1, e1500047 (2015).  Acknowledgements: This perspective was inspired in part by a workshop held at the Carnegie Institution for Science in Washington DC, Nov. 9th – 15 h 2015 and we thank the contributors to this conference. 

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Beyond prebiotic chemistry

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