Transcript On the Emergence of Biological Complexity:

Seeking the Evolutionary Roots of
Horizontal Gene Transfer (HGT)
Addy Pross
Department of Chemistry, Ben Gurion University of the Negev
Be’er Sheva, Israel
HGT & LUCA Conference,
The Open University, Milton Keynes, Sept. 4-6, 2013
Biology in Crisis
Carl Woese
“Biology today is no more fully understood in principle
than physics was a century ago…. the guiding vision
has reached its end …. a new, deeper, representation of
reality is called for”
Bottom line: 150 years after Darwin, we still don’t
adequately understand biology’s essence and the nature
of the evolutionary process
Central HGT & LUCA Questions
 How fundamental is HGT to the evolutionary process?
 What was the nature of LUCA?
 What does Woese’s ‘Darwinian threshold’ actually
represent?
 Is the evolutionary process best represented by a tree
or a web?
 Is HGT Lamarckian or Darwinian?
Systems Chemistry
A new area of chemistry
Systems Biology -‘top-down’
Systems Chemistry -‘bottom-up’
Deals with simple replicating chemical systems and
the networks they establish
G. von Kiedrowski, S. Otto, P. Herdewijn, J. Syst. Chem. 2010
Regular
Chemistry
Systems
Chemistry
Non-replicative
Simple
replicative
Biology
Complex
replicative
To understand how something works, look at
a simple version
Biology
Systems chemistry
Systems Chemistry:
Merging Chemistry and Biology
Non-Life
Chemical
phase
?
Biological
Simple phase
Complex
Life Darwinian Life
theory
One single physicochemical process
Replication reaction - the underlying connection
A. Pross, J. Syst. Chem. 2011
Molecular Replication
A + B + C + …..
T
T
Molecular
Replication
e.g., nucleic acids, peptides, synthetic molecules
Template mechanism
S. Spiegelman, 1967
G. von Kiedrowski, 1986
L. Orgel, 1987
J. Rebek, 1994
M.R. Ghadiri, 1996
G. F. Joyce, 1997
Replication Reaction is
Autocatalytic
Autocatalysis - can exhibit exponential growth
 79 replication cycles would convert a single
molecule to a mole (279 ~ 6. 1023).
 a further 83 cycles would generate a mass
equal to that of the earth, 1027g!
Replication is unsustainable
T. Malthus, An Essay on the Principle of Population, 1798
Stability
A system is stable if it is persistent, unchanging
over time.
Thermodynamic Stability – an inherent property of a
chemical system, one that is quantifiable.
Second Law of Thermodynamics:
All systems tend from less stable to more stable
An Alternative Stability Kind
Dynamic Kinetic Stability (DKS)
A stability kind associated with replicating systems
(chemical or biological) that display persistence
Can underpin a general theory of evolution and help
identify the driving force for the evolutionary process
Pross et al. 2004-2013
Dynamic Kinetic Stability (DKS)
Replication is unsustainable, therefore for stability
rate of replicator formation =~ rate of decay
dX/dt = kXM - gX
X = replicator conc.
M = monomer conc.
k,g = rate constants.
A. Lotka, 1910
dX/dt = 0 would define
a steady state population
If a replicating system is stable
then its stability is of a dynamic kinetic kind
Stability in ‘Regular’ and
Replicative Worlds
 ‘Regular’ chemical systems are stable
because they DO NOT react.
 Replicating chemical systems are stable
(persistent) because they DO react – to make
more of themselves!
DKS would apply to all stable replicating systems,
biological and chemical.
A.Pross, Pure Appl. Chem. 2005
Selection Rules in ‘Regular’
Chemical and Replicator Worlds
‘Regular’ Chemical World:
Thermodynamically
Less Stable
Thermodynamically
More Stable
Replicator World:
Dynamic kinetically
Less Stable
Dynamic kinetically
More Stable
A. Pross, J. Syst. Chem. 2011
A. Pross, Pure Appl. Chem. 2005
Example of Replicator Selection Rule
activated
nucleotides
Qb RNA
Mutant RNA
74 replication
cycles
(4500 b)
Sequence of events:
Replication
Mutation
(220 b)
S. Spiegelman, 1967
Selection
Evolution
Faster RNA drive slower RNA into extinction
In stability terms:
From DK less stable to DK more stable
Identifying the Driving Force
for Evolution
Simple
replicating
entity
Chemical
phase
Biological
Simple phase
Life
Complex
Life
Drive toward greater DKS
One single physicochemical process
What actually takes place during evolutionary process?
A. Pross, J. Syst. Chem. 2011
Evolutionary Process
Characterized by Complexification
A clear tendency toward complexification during
evolution – both chemical and biological
Chemical (molecular) level:
Molecular replicating system
simple life
Biological level:
prokaryotes
ecological networks
eukaryotes
multicell organisms
Extent of Complexification
During Evolution
Chemical
Biological
Simple
Simple
Complex
phase
phase
Replicating
Life
Life
System low complexity
high complexity
One continuous process
Drive toward greater DKS
low complexity – low stability
high complexity – high stability
A. Pross, J. Syst. Chem. 2011
General Theory of Evolution
All stable (persistent) replicating systems will
tend to evolve (primarily by complexification)
toward systems of greater DKS.
Extended theory embraces both biological and
chemical systems
A. Pross, J. Syst. Chem. 2011
Darwinian concepts - Particular applications
of broader chemical concepts
Darwinian Concepts
Chemical Concepts
natural selection
kinetic selection
fitness
survival of the fittest
dynamic kinetic
stability (DKS)
drive toward greater
DKS
Darwinian concepts firmly rooted in chemistry
Biology – a complex manifestation of replicative
chemistry
A.Pross, J. Syst. Chem. 2011
A.Pross, Chem. Eur. J. 2009
Global Characteristics of Living
Systems Explained by DKS
 Diversity
 Functional complexity
 Dynamic character
 Far-from-equilibrium state
 Teleonomy (purposeful nature)
 Homochiral character
Origin of Diversity
Diversity – a central element of Darwinian
theory
Darwin’s Two Principles
Principle of Natural Selection - many become few
Principle of Divergence - few become many
Topology of ‘Regular’ Chemical and
Replicator Spaces
Thermodynamic
sink
‘Regular’ (thermodynamic)
Space
Convergent
Replicator (kinetic)
Space
Divergent
Replicator Space – Open, circumstantial
Topology of replicator space explains diversity
Clarifies Darwin’s Principle of Divergence
A. Pross, J. Syst. Chem. 2011
Implications of Different
Topologies
Regular systems:
History inaccessible
Future predictable
Replicators:
History accessible
Future unpredictable
N. Wagner, A. Pross, Entropy 2011
A. Pross, Pure Appl. Chem. 2005
Diversification at Chemical Level
1) Replication (VGT) + mutation
Qb RNA
(4500 b)
activated
nucleotides
Mutant RNA
74 replication
cycles
(220 b)
S. Spiegelman et al., PNAS, 1967
2) HGT – mechanism for diversification that is not
directly connected to replication step.
HGT already evident at chemical level.
Molecular HGT in Action
N. Lehman et al., Nature 2012
(fig: Attwater & Holliger, Nature 2012)
Cooperative cycle out-replicates individual cycles.
An expression of HGT at molecular level!
HGT – not just mechanism for variation but for
complexification
Complexification during Evolutionn
Chemical
Biological
Simple
Simple
Complex
phase
phase
Replicating
Life
Life
System low complexity
high complexity
One continuous process
Drive toward greater DKS
low complexity – low stability
high complexity – high stability
A. Pross, J. Syst. Chem. 2011
Answers to Central HGT Questions
How general is HGT in evolution?
HGT crucially important as a major mechanism for
diversity and complexification. Operates along the
entire evolutionary process.
Simple replicators – simple HGT
molecular level: transformation
More complex replicators – more complex HGT
prokaryotic level: conjugation, transduction
eukaryotic level: sexual selection
HGT lesson - variation is not restricted to the replicative
step. Nature is opportunistic! Lamarckian character
Nature of LUCA
Was LUCA organismal or communal?
Is extant life organismal or communal?
Plants cannot fix nitrogen without bacterial assistance
Humans are 90% bacterial by cell count
Bacteria live in colonies (communicate chemically and
coordinate actions eg, in biofilm formation)
Animals seem to be individual, but actually network
dependent, replicatively incomplete
Conclusion: life is a network phenomenon, intrinsically
communal
Systems Chemistry Viewpoint
Systems chemistry studies indicate that network
formation (complexification) is the primary
mechanism for increasing DKS
Central mechanism of abiogenesis would have been
network formation.
Conclusion: LUCA was communal because evolution
is fundamentally a networking process – right from its
origins.
Biology overemphasizes life’s individuality.
Dynamic Kinetic Stability (DKS)
Stability in replicative world (DKS) is not associated
with individuals, only with populations.
Individual replicators have no DKS.
Individuals don’t evolve, populations do!
Is LUCA a meaningful concept?
LUCA - associated with Darwinian Threshold
Darwinian Threshold = Speciation Threshold
LUCA – diverse population of replicatively coupled
entities that preceded speciation
Primal speciation: the point at which
replicative networks physically separated,
began to utilize available resources
differentially, and began to evolve
independently
Key Conclusions
DKS - the conceptual bridge between Chemistry and
Biology.
• Unifies abiogenesis and biological evolution
• Integrates Darwinian theory into general chemical
theory
• DKS – the driving force for evolution
• Systems Chemistry – the road to greater biological
understanding. HGT and LUCA can be better
understood by seeking their roots in chemistry
• Scientific reduction in biology is alive and well!
Carl Woese’s prophesy of revolution in biology 32
may be realised - through Systems Chemistry.
Thank you for your attention!