The Major Transitions in Evolution: A Physiological

Perspective

Andrew H. Knoll

Harvard University

1. Replicating molecules Populations of molecules in

compartments2. Independent replicators chromosomes3. RNA DNA and proteins4. Prokaryotes Eukaryotes5. Asexual clones Sexual

reproduction6. Single cells Multicellular

organisms7. Solitary individuals

Colonies with non-reproductive castes

8. Primate societies Human societies (language)

To

Physiological/Metabolic Major Transitions

Autotrophy1. From reliance on abiotic synthesis to chemosynthesis2. From chemosynthesis to photosynthesis3. From anoxygenic to oxygenic photosynthesis4. From reliance on environmental N to nitrogen fixation

Heterotrophy5. From fermentation to respiration6. From anaerobic respiration to aerobic respiration7. From absorption of organic molecules to phagocytosis8. From diffusion to bulk transport 9. Technology

Photosynthesis

Van Niel Equation: CO2 + 2H2A CH2O + H2O + 2A

Electron donor can be water, but also Fe2+, As3+, H2S, H2, organic molecules

http://en.wikipedia.org/wiki/File:Z-scheme.png

Primary production, limited by electron supply before oxygenic

photosynthesis?

Canfield et al. (2006)

Nealson (1997)

What about earlyheterotrophy?

Nealson (1997)

1. Importance of Fe in Archean carbon cycle

2. Limitations on chemoautotrophy imposed by oxidant pool

Conceptual model of Archean and iron formation deposition,

derived from the biological oceanic iron cycle.

Fischer and Knoll (2009)

Several lines of evidence indicate

oxygenation 2.4 Ga

• Banded iron formation • Detrital uraninite, siderite,

and pyrite• Paleosols• Sulfur isotopes

Our hero

Falcon et al. (2010)

1332/1232

2211/2057

3028/2519

Plastids

Heterocysts

N-fixers

What drove oxygenation?

Assumption of cyanobacterial origins: 3500/2700 Ma

How much O2 accumulated?Lyons and Reinhard (2009)

Maliva et al. (2005)

Nealson (1997)

Accumulating oxygen alters carbon cycle and its constituent metabolisms

After Anbar and Knoll (2002)

Scott et al. 2008Shen et al. (2003)

Brocks et al. (2005)

De Duve (2007)

The Eukaryotic Cell

1. Qualifies as a major transition in the scheme of MS & S.2. What are its metabolic or physiological consequences?3. Briefly consider phagocytosis and the acquisition of energy metabolisms.

Phagocytosis

1. 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)

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

Innovation vs. limitation.

Consequences of redox structure for eukaryotic organisms?

• 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

Martin et al. (2003)

Johnston et al. (2009)

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)

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)

Subsurface sulfide decline

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

Courtesy of N. Butterfield

Courtesy of Phoebe Cohen

Porter et al. (2003)

More scales…P. Cohen, PhD thesis

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

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

Diffusion and metabolism

• 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)

Knoll and Hewitt (2011); left after Runnegar (1991)

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)

Size

Nutrient/Signal Gradient

Differentiation

Development feeds back on physiology

With time, cross a functional threshold that promotes the diversity (evolvability?) of complex multicellular clades.

MAKES ECOLOGICAL FEEDBACKS POSSIBLE.

Size

Nutrient/Signal Gradient

Differentiation

Development feeds back on physiology

With time, cross a functional threshold that promotes the diversity (evolvability?) of complex multicellular clades.

MAKES ECOLOGICAL FEEDBACKS POSSIBLE.

PO2

When did atmosphere/ocean begin its transition to a more modern state?

Derry et al. (1992)

Canfield and Teske (1995)

Scott et al. (2008) Dahl et al. (2010)

24-isopropylcholestane; Love et al. (2009)

(??)

Ediacaran-Cambrian Animal Radiation

The Evolutionary

Present

Peter Brewer (MBARI)

• Major transitions in physiology both track and drive environmental changes in Earth history

• Might characterize evolutionary trajectories wherever life emerges

The Punch Line

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