Oxygen and Functional Evolution of Organismsby Miquel Riera-Codina (mrieracodina@ub.edu)

Men and animals live thanks to the oxygen in the air. Oxygen is considered to be asource of life. But the earliest atmosphere did not contain oxygen. How and when didthis gas appear? What influence did it have over the evolution of animals? This articleattempts to point out some aspects which might lead us to think that oxygen had animportant role in the development of the complexity of living organisms, in a similarway perhaps to the way that the use of oil has facilitated the development of acomplex human society.

In the XVIIIth century, Lavoisier and Laplace thought that life was like combustion, that is to saythat in the same way that wood produces heat when oxidized by air, animals oxidize organic matterto obtain energy (to heat themselves, grow and move).

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The complex structure of living organisms needs energy to sustain it (second principle of thethermodynamics). Organisms are highly improbable structures which are maintained thanks tometabolic energy. However, the development of organisms with increasing functional complexityrequired the development of energetic systems which were progressively more efficient. Lets try nowto explain how oxygen could condition the evolutionary process in animals.

The first organisms developed without O2.

Respiration, and therefore life forms as we know them now, could not have developed in the earlieststages of the Earth’s formation since the atmosphere of the primitive Earth did not contain oxygen.The presence of this gas is a relatively recent fact (from 1,5 to 2 billion years ago). What influence,therefore, did oxygen have in the development of organisms? Why were complex cells not able toassociate in multicellular organisms before the appearance of oxygen? First let's notice that it isdifficult for us to assimilate and appreciate very long periods of time, so perhaps it would be usefulto consider a new relative time scale much closer to that of our daily life. Imagine then that the entirehistory of the Universe has occurred in the space of one year, between, for example, January 1st

and December 31th of 2003. Based on this time scale, which will represent our referencecalendar, on the first of January the Universe was formed, but it would not have been untilSeptember 14 (or approximately 4,6 billions of years ago) that the Earth was formed. By then theatmosphere was rich in nitrogen, hydrogen, carbon dioxide, methane and water vapour among other,but did not contain oxygen.

Relative date Evolutive event Functional evolutionJanuary 1 Universe formationSeptember 14 Earth

formationAbiotic (biochemical) evolution

October 15 Development of anaerobicmetabolism.

November 1 Anaerobic photosynthetic bacteria(do not produce O2 )

November 12 Photosynthesizers that produce O2

December 1 Development of O2-rich atmosphere2:Formation of ozone layer

Development of aerobic metabolism

December 8 First eukaryotes (complexcells)

Consolidation aerobic metabolism

December 16 First multicellularanimals

Development of organs and tissues

December 19 First vertebrates (primitivefishes)

Development of sistems of functionalcoordination

December22 to 24

Land colonization: first amphibian,Reptiles, and flyinginsects

Development of functionalcomplexity

December 26 First birds and mammals Encephalic development.Centralized functional regulation,higherfunctions

December 29 First primates Higher encephalic functions

De 31 22h 36’ Firsthominides

Cultural development

-23h 46’ Man uses fire

-23h 59’ 35’’ First village

-23h 59’ 56’’ Christ isbornDevelopment of modern scienceand industry

Ozone hole-23h 59’ 59’’

.

Contrary to what is shown in themovies, the landscape would havehad a quite different aspect to thatfound in the present arid areas, itprobably had a greyish appearance,like volcanic zones, because the rockswere not oxidized on entering incontact with the atmosphere.

Already in the 1920’s Oparin and Haldane explained that in such conditions important biochemical reactionswould occur that would lead to the formation of organic compounds (abiotic or chemical evolution).However life did not appear until approximately October the 15th of our calendar (about 3.4 billion years ago).

Some tiny vesicles, which were able to develop insidecoordinated reactions to obtain energy, appeared in theseas. Thus, the first form of living organism appeared, thecell. These first cells were very simple (protobionts or“metabolic vesicles”, and eubions, when incorpored agenetic system, true life forms) and they evolved byincreasing their internal complexity becoming organismsnot dissimilar to the present bacteria. They had to obtainthe energy necessary to support their internal level oforganization by oxidation of organic compounds(heterotrophs), by the oxidation of inorganic substances(chemotrophs) or by the oxidation of the organiccompounds previously synthesized by means of luminousradiation (autotrophs).

Anyway one thing is clear, the oxidation must have been produced in the absence of O2 (anaerobes), hencethe final acceptor of electrons could either have been an inorganic substance (for example sulphate-reducingmicrobes, see Shen et al. in Nature, 410, 77-80, 2001) or a partially oxidated organic compound (fermentation),but in either case this must have been with a reduced oxidative capacity in comparison with that of the O2.This type of metabolism produces little energy and therefore these organisms could not evolve toward verycomplex forms. In any case, they began to proliferate into the oceans and developed more complex andefficient chemical reactions (metabolic evolution).

Below is shown a nice model for evolution of primitive cells extracted from http://www.gly.uga.edu/railsback/1122main.html

The oxygen appears: the first great atmospheric “contamination”

Returning to our calendar, on November 1 some cells begin to use sunlight to obtain energy by photosynthesis(like the present green and purple sulphur bacteria which are anaerobics and do not produce O2) and later someof these cells developed an oxygen-producing photosynthesis (like blue-green algae). This mechanism wasmore suitable energetically and therefore this type of cell began to proliferate in the seas, this enlarged quicklythe production of oxygen which thus began accumulating in the primitive atmosphere. 1.8 million years ago (byDecember 1) the quantity of atmospheric oxygen already was similar to the present.

The accumulation of oxygen in the atmosphere hada spectacular effect on the landscape. The rocksbegan to oxidize and become red and yellowish,the landscape was filled with colour similar to thepresent arid areas. In fact oxygen represented thefirst large scale environmental pollution due to theaction of the living organisms.

In addition, in the higher layers of the atmosphere, a gas was formed which derived from the oxygen: ozone.This gas intensely absorbs the ultraviolet radiation from the sun, which destroys the living organisms; thereforethese primitive cells could reach the upper layers of the seas and have access to oxygen. Some of themdeveloped metabolic pathways to utilize this new gas. We are not here going to enter into the interestingmolecular adaptations that would need to be produced to metabolize the O2, we only wish to note that by

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Aaerobic bacteria Anaerobic bacteria

Process of close association

“Eukaryotic” cell (with mitochondries)

aerobic respiration cells could obtain much more energy. Organisms with this high energy performance couldevolve into more complex forms. As a result, a new cellular organization appeared, the eukaryotic cell. Theseare complex cells, with a nucleus and organelles, with an aerobic metabolism already consolidated whichforms part of all multicellular organisms. This happened approximately 1.4 billion years ago (December 8,from our calendar).

An interesting hypothesis about theformation of eukaryotic cells based onthe close association between twobacteria with complementarymetabolisms has been recentlyproposed. First, both cells tend to begrouped because the hydrogen and thecarbon dioxide produced by theaerobic bacteria is used by theautotrophic methane producer. Later,a close association is promotedbecause this favours a betterexchange. Finally, a cell is includedas an organelle (mitochondria) in theother cell. The two metabolisms areultimately fused in a final, moreefficient, aerobic metabolism.

The aerobic metabolism is consolidated in eukaryotic cells: the road to multicellular forms is open.

Eukariotes having a greater energy performance could develop locomotion and systems relation. Near thesurface of the seas, where there was more oxygen, cells may have begun to associate in coordinated groups,forming the first multicellular-like organisms.

Coelenterates are very simpleanimals, their cells are notdifferentiated in specializedtissues.

Multicellulars are more complex and thus more energy is needed for maintaining their level of organization: thedevelopment of an aerobic metabolism would have been crucial for their formation. These new organisms tookadvantage of the efficiency of aerobiosis, began to proliferate and evolve to greater size and more complexforms, and developed specialized tissues and organs. The first multicellulares appeared 670 million years ago.550 million years ago invertebrates appeared with the skeletal structure that gave rise to the great proliferationof forms during the Cambrian period. Very soon after the first vertebrates appeared (primitive fish: Agnathaand Placoderms) although they were not diversified until the Devonian period (400 million years ago). All thisoccurred only in approximately a week of our calendar (12-20 December).

The pressure of the sea population stimulates the development toward land and air respiration. The airhas a high oxygen content.

Then another notable moment in the evolution of organisms occurred. The explosion of living forms filledthose oceanic areas more suitable for life, so some animals were pushed to less stable zones, such as marshes,rivers, lakes and flooded areas. Warmer and rainier periods enlarged the extensions of flooded land in the formof mangrove swamps and marshy zones. These areas contain hot water which is very poor in oxygen, soanimals that lived there had to adapt to the use oxygen from the air, thus facilitating the transition of lifetoward land.

The terrestrial environment is much more changable than the marine one, thus animals had to develop an airbased respiration system, and mechanisms to insulate them from environmental variations, and this involvedthe development of mechanisms of physiological regulation. However, animals had access to a higher energysource since air contains much more O2 than water. Again, therefore, it was the oxygen that provided theenergy to allow animals to adapt to changing environments and to develop to new evolution stages: thedevelopment of complex regulation systems. Thus, the amphibians appear and a little later the reptiles colonizethe land (from Permian to Cretácico, 280 to 80 million years ago). In the Triásico already primitive mammalsexisted although they would not diversify and proliferate until Cretácico (140 million years ago).

Mammalian (the first mammals were small but developed important homeostaticmechanisms for functional regulation) and birds developed large functional regulatoryand coordination centres in the encephalus (Prosencephalus) and these allowed them toattain greater independence from the changing environment. Their encephalus acquiredfunctions of auto-control and conscious conduct.

From the appearance of the first hominids in Africa 11 million years ago (31 from December at 10 o'clock

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Photolysis of CFC Cyclic process of ozone destruction

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hours and 30 minutes of the night of our calendar) things began to move rapidly. Thus at eleven o'clock in theevening our ancestors had already learned to work with stone tools, by four minutes to twelve they had learnedto use the fire, the first village appeared at half a minute to midnight, at 4 seconds before the stroke of twelveChrist was born, and one second before man developed the scientific method and began the modern industrialrevolution. Mankind has made use, for good or for ill, of this last second to develop all we now know asscience and modern industry.

The modern industry release to atmosphere chlorofluocarbons.

One of the most important consequences of industrial development has been the destruction of the ozone layerthrough accumulation of chlorofluocarbon compounds (CFC) produced by modern industry. It was thoughtinitially that these compounds would be ideal since they appeared not to react and therefore not to pollute. Sothey were produced and released into the atmosphere in large quantities. But slowly the CFC ascended throughthe atmosphere and accumulated in the stratosphere.

There, in extreme temperature conditions ( morethan 60-80ºC below zero) and intense sunlight(present in the Antarctic during relatively longperiods of time), these gases become reactiveand break down the ozone in oxygen. Theproblem is that a cyclic process can be occurand thus each molecule of CFC continuouslydestroys the ozone.

It would be paradoxical if an organism which in part has arisen thanks to the formation of the ozone layer inancestral periods of the Earth, now returns the planet to its initial conditions.In the CFC case international measures have been taken and it seems that the reduction in emission of CFCs isunder control. We should keep in mind, nevertheless, that the process has great inertia and at present largequantities of these compounds released by the industry of the eighties are still arriving in the stratosphere . Willwe be able to really stop the destruction of the ozone layer by the CFCs? Will we be able, know how to orwant to act to avoid future alterations in the environment? Keeping in mind the giddy changes that are beingproduced in the environment we should be cautious in introducing any alterations that can induce effects withgreat inertia. Which history will we be able to write for January 1, 2004 of our calendar?

Related links• Cellular evolution (Chapter 11). In EVOLUTION FACTS, INC. BOX 300 - ALTAMONT, TN. 37301 .

http://evolution-facts.org• The Progenote. Draft of an article to appear in the ENCYCLOPEDIA OF MOLECULAR BIOLOGY.

http://www.sp.uconn.edu/~gogarten/progenote/progenote.htm• Webpage for Dr. Bruce Railsback's lecture section. In Earth's History of Global Change, University of

Georgia, Department of Geology. http://www.gly.uga.edu/railsback/ 1122main.html• Cellular genesis. In The Harbinger symposium, "Religion & Science," Alabama Humanities Foundation,

http://www.theharbinger.org/articles/ rel_sci/fox.html• The Origin of Higher Life Forms. http://www.amazingdiscoveries.org/ lifeforms.html

Books

• Avers, Charlotte J. Cap. 18 Cellular and molecular evolution. In Molecular Cell Biology. Ed. Addison-Wesley (1986)

• Montero, F. Y Morán, F. Biofísica. Procesos de autoorganización en Biología. Ed. EUDEMA, 1992.• Losada, M., Vargas, M. A., De la Rosa, M.A., Florencio, F.J. Los elementos y moléculas de la vida.

Introducción a la química biológica y biología molecular. Ed. Rueda, 1999.• Ecología y Evolución. En História Natural. Ed. Carroggio. 1990• Tomo 15 Registre fòssil. En Història natural dels països catalans. Ed. Fundació Enciclopèdia Catalana,

1989.

Articles

• Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature, 392, 37-41 (1998)• Castresana, J. & Saraste, M. Evolution of energetic metabolism: respiration-early hypothesis. TIBS, 20,

443-447 (1995)• López-García, P. & Moreira, D. Metabolic symbiosis at the origin of eukaryotes. TIBS, 24, 88-93 (1999)• Solomon, S. Progress towards a quantitative understanding of Antarctic ozone depletion. Nature, 347, 347-

353 (1990)