The Major Transitions in Evolution: A Physiological Perspective

1. The Major Transitions in Evolution: A Physiological Perspective Andrew H. Knoll Harvard University

2. 1. Replicating molecules  Populations of molecules in compartments 2. Independent replicators  chromosomes 3. RNA  DNA and proteins 4. Prokaryotes  Eukaryotes 5. Asexual clones  Sexual reproduction 6. Single cells  Multicellular organisms 7. Solitary individuals  Colonies with non- reproductive castes 8. Primate societies  Human societies (language) To

3. Physiological/Metabolic Major Transitions Autotrophy 1. From reliance on abiotic synthesis to chemosynthesis 2. From chemosynthesis to photosynthesis 3. From anoxygenic to oxygenic photosynthesis 4. From reliance on environmental N to nitrogen fixation Heterotrophy 5. From fermentation to respiration 6. From anaerobic respiration to aerobic respiration 7. From absorption of organic molecules to phagocytosis 8. From diffusion to bulk transport 9. Technology

4. Photosynthesis http://en.wikipedia.org/wiki/File:Z-scheme.png Van Niel Equation: CO2 + 2H2A CH2O + H2O + 2A Electron donor can be water, but also Fe2+, As3+, H2S, H2, organic molecules

5. Primary production, limited by electron supply before oxygenic photosynthesis? Canfield et al. (2006)

6. What about early heterotrophy? Nealson (1997)

7. Importance of Fe in Archean carbon cycle • Limitations on chemoautotrophy imposed by oxidant pool Nealson (1997)

8. Conceptual model of Archean and iron formation deposition, derived from the biological oceanic iron cycle. Fischer and Knoll (2009)

9. Several lines of evidence indicate oxygenation 2.4 Ga • Banded iron formation • Detrital uraninite, siderite, and pyrite • Paleosols • Sulfur isotopes Our hero

10. Plastids 1332/1232 Falcon et al. (2010) What drove oxygenation? 2211/2057 Heterocysts Assumption of cyanobacterial origins: 3500/2700 Ma 3028/2519 N-fixers

11. How much O2 accumulated? Lyons and Reinhard (2009) Maliva et al. (2005)

12. Accumulating oxygen alters carbon cycle and its constituent metabolisms Nealson (1997)

13. Brocks et al. (2005) After Anbar and Knoll (2002) Shen et al. (2003) Scott et al. 2008

14. The Eukaryotic Cell • Qualifies as a major • transition in the • scheme of MS & S. • What are its metabolic • or physiological • consequences? • 3. Briefly consider • phagocytosis and • the acquisition of • energy metabolisms. De Duve (2007)

15. Phagocytosis • Enables particle capture, including bacterial and protistan cells (and small animals) • 2. Introduces predation as a • key ecological process • 3. Changes physical nature of organic C acquisition, but not metabolic means of generating energy • Image shows amoeba eating a yeast cell; • Pierre Casson (http://www.forschung3r.ch)

16. In eukaryotes, energy metabolism is largely the product of endosymbiosis, incorporating bacterial cells. -- Aerobic respiration  mitochondria  proteobacteria -- Oxygenic photosynthesis  chloroplast  cyanobacteria Innovation vs. limitation.

17. Consequences of redox structure for eukaryotic organisms? Johnston et al. (2009) Martin et al. (2003) • Mitochondria must have arisen in a global setting where marine oxygen levels were extremely low and sulfide levels were high. Furthermore, the first ~1 billion years (at least) of eukaryote diversification occurred in a marine environment marked by low oxygen, widespread anoxia and high sulfide. • Hypoxia/anoxia • Sulfide toxicity (interfere with cytochrome c oxidase in mitochondria) • Fixed nitrogen availability

18. Photosynthetic eukaryotes in mid-Proterozoic oceans 0.5 million or more species today In mid-Proterozoic oceans, problematic Capacity to fix carbon was not accompanied by the ability to fix nitrogen In mid-Proterozoic oceans, limited fixed nitrogen in photic zone. Ecological advantage to photoautotrophs able to fix N2. Butterfield (2000)

19. Mitochondriate eukaryotes in mid-Proterozoic oceans • Systemic inhibition by sulfide – interferes with cytochrome c oxidase function in mitochondria • Widespread sulfide in mid-Proterozoic oceans may have challenged eukaryotes in many marine environments. • Mitochondrial adaptation to anoxic metabolism occurs (hydrogenosome, mitosome), but is a one way street • When did environmental challenges of sulfide and fixed nitrogen fade? Porter and Knoll (2000)

20. Subsurface sulfide decline • Johnston et al. (2010) – Ferruginous subsurface waters begin at least 800 Ma, concomitant with widespread rifting of supercontinent Rodinia

21. Porter et al. (2003) Courtesy of Phoebe Cohen Courtesy of N. Butterfield

22. More scales… P. Cohen, PhD thesis

23. Multicellularity • A major transition in MS & S scheme • But a common transition – fully 1/3 of the 119 major eukaryotic clades recognized by Adl et al. (2005) have evolved simple multicellularity; most have limited diversity • Six (possibly 7) clades have evolved complex multi-cellularity; 95% of all described eukaryotic species

24. 1. In complex multicellular organisms, only a subset of cells are in direct contact with the environment.2. In organisms with 3-D multicelluarity, diffusion will strongly affect both metabolism and development. The Problem of Diffusion

25. Diffusion limits size attainable at any given pO2 • Circumventing diffusion: • Mechanisms to enhance directional cell-cell transfer (plasmodesmata, gap junctions, incomplete septation) • Specialized cell and tissue types for bulk transfer (phloem, trumpet hyphae, circulatory systems) Diffusion and metabolism Knoll and Hewitt (2011); left after Runnegar (1991)

26. Diffusion and development • Only surface cells directly encounter environment • Gradient in concentration of signaling molecules develops • Gradient develops in diffusible environmental factors that induce cell differentiation in unicellular eukaryotes modification (e.g., nutrients, oxygen) Schlichting (2003)

27. Development feeds back on physiology Size Nutrient/Signal Gradient Differentiation With time, cross a functional threshold that promotes the diversity (evolvability?) of complex multicellular clades. MAKES ECOLOGICAL FEEDBACKS POSSIBLE.

28. Development feeds back on physiology Size PO2 Nutrient/Signal Gradient Differentiation With time, cross a functional threshold that promotes the diversity (evolvability?) of complex multicellular clades. MAKES ECOLOGICAL FEEDBACKS POSSIBLE.

29. When did atmosphere/ocean begin its transition to a more modern state? Canfield and Teske (1995) Derry et al. (1992) Scott et al. (2008) Dahl et al. (2010)

30. Ediacaran-Cambrian Animal Radiation (??) 24-isopropylcholestane; Love et al. (2009)

31. The Evolutionary Present Peter Brewer (MBARI)

32. The Punch Line • Major transitions in physiology both track and drive environmental changes in Earth history • Might characterize evolutionary trajectories wherever life emerges

33. Thanks to … • Members of the Knoll lab (especially Tais Dahl, Ben Gill and Phoebe Cohen) • Colleagues further afield, especially Dave Johnston and Don Canfield • Funding from NSF, NASA Exobiology, and the Agouron Institute