Cyanobacteria - superheroes of evolution

The first plants, photosynthetic cyanobacteria, are still
abundant in a great variety of forms today and account for
about 20-30% of the current oxygen production in the
oceans.  photo by Mary Cousins cc by SA 3.0

Though it's not obvious from the name, cyanobacteria are photosynthetic organisms.  They were actually called "blue-green algae" until it became evident that they are prokaryotes related to other bacteria.  They thus have a simpler cell structure than the "true" eukaryotic algae and higher plants.

The ancestors of modern cyanobacteria invented photosynthesis over 3 billion years ago, or I should say they assembled it from processes obtained through horizontal gene transfer from at least three different ancient bacteria.  (See "The first plants") Earlier bacteria that harvested sunlight created carbohydrate, but the cyanobacterial process also releases releases oxygen as a byproduct, and therein lies the most important part of the story.

Cyanobacteria, such as this filamentous Oscillatoria were
classified as algae until their prokaryotic nature was discovered.
Photo by Wiedehopf20. CC SA 4.0 International

Chroococcus is a cyanobacterium in which
cells divide within a gelatinous  matrix. 
Photo by Xvazquez CC by 3.0 unported.

For the first 2 billion years of their existence, cyanobacteria alone served as the base of the world's food chain, providing vast quantities of carbohydrate to feed the rest of life.  That in itself was a stupendous contribution by this group of organisms, but it was the production of oxygen that changed the world forever, making more complex plants, fungi, and animals not only possible, but obligatory and inevitable. By producing oxygen as a byproduct, cyanobacteria converted the primordially anaerobic world into an aerobic one, which both enabled and forced the evolution of a variety of organisms that could note only tolerate the toxic effects of oxygen, but also put it to use through aerobic respiration. At the same time, countless and largely unknown anaerobic organisms became extinct. It may have been the first mass extinction of life on Earth.  That, however, didn't happen right away - there was a 2 billion year delay - for a simple reason we'll see shortly.

All protists, animals, fungi, and higher plants are composed of eukaryotic cells.  Bacteria and archaeans have the much smaller and structurally simpler cell structure we call prokaryotic. Though the name “eukaryote” emphasizes the presence of a true nucleus, these more advanced cells have additional complex organelles, internal membrane systems, and a sophisticated cytoskeleton that controls cell shape, cell and nuclear division, and the movement of organelles and materials within the cell.  Such complex cells require a lot of energy for all this internal activity, and so could not have existed until oxygen was available.

When oxygen did finally become abundant in the seas, aerobic bacteria evolved, first to protect themselves, and then to harness the oxidative power of oxygen to break food materials more completely. What a boon that was!  Anaerobic respiration can squeeze only 2 ATP molecules from a molecule of glucose, while aerobic respiration yields 38!

The first eukaryotic cell evolved as a flexible, amoeba-like archaean
ingested aerobic bacteria, which evolved into  mitochondria. Later,
cyanobacteria were captured by a primitive eukaryote, and became the
chloroplasts of the first true algae.

Once aerobic bacteria evolved, another kind of ancient prokaryote took a shortcut to adapt to the oxygen-rich world.  This one, an
archaean, had already shed the rigid cell wall that surrounds most prokaryotes, and with its naked, flexible wall it could surround other cells and bring them inside for digestion.  It was essentially a primitive amoeba with a rudimentary cytoskeleton.
Such a cell eventually met up with an aerobic bacterium, related to modern purple non-sulfur bacteria, and took it inside.  Instead of digesting the bacterium, however, a truce developed between the two cells and a deal was struck.  The host cell provided food to the captured aerobic bacterium, and the bacterium in turn absorbed oxygen, used it to break down the food, and paid rent to the host cell in the form of ATP molecules.  That captured aerobic bacterium evolved into the energy–processing organelle we call the mitochondrion, and that symbiotic union was the first eukaryotic cell.  Incidentally, but also of huge significance, cyanobacteria were also engulfed by some early eukaryotes and became the chloroplasts we find in algae and higher plants.

This formation of the first eukaryotic cell has been considered by some scientists to have been particularly unlikely, and that only by chance did life on Earth therefore progress from the prokaryotic to the eukaryotic level of complexity.  In his Scientific American article of September 2018 ("Alone in the Galaxy"), John Gribbin says “it is a measure of how unlikely such a single fusion of cells was that it took two billion years of evolution to occur.” (italics added for emphasis.)  This implies that the evolutionary progress of life was stalled for two billion years and may never have gone on to form eukaryotic cells (and eventually humans), if this rare fluke of an event hadn’t happened.  Gribbin and others (including the late Stephen J. Gould) believe humans exist in the universe only because of a series of such flukes. (see references below).

As I proposed in my last post (Of cacti and humans – are certain life forms inevitable?) the evolution of life did not proceed through miraculous flukes, but rather inevitably through predictable processes. In the first place, symbiosis among prokaryotes is exceedingly common.  In fact, only two months after Gribbin’s article, another article showed up in Scientific America, which suggested that symbiotic cooperation among prokaryotes might be the rule rather than the exception (see “Team Players,” by Jeffrey Marlow and Rogier Braakman, Scientific American, November, 2018). In addition, “The Runes of Evolution, by Simon Conway Morris (2015), provides abundant examples of ways in which symbiosis occurs among microorganisms, as well as providing a veritable encyclopedia of convergent evolution throughout the kingdoms of life. So it is really quite predictable that a flexible, carnivorous archaean would sooner or later run into an aerobic bacterium, ingest it, and eventually domesticate it into an internal organelle that would help it extract more energy from food items. 

So what was the real reason for the 2 billion year delay?  Iron. At the beginning, there was a huge amount of dissolved iron in the oceans as well as in the surface rocks.   When exposed to oxygen, iron rusts, as anyone who has left tools outside too long knows. Technically speaking, this early iron was in its reduced state, and when exposed to oxygen it became oxidized. The oxidized form of iron, however, is not soluble in water, so it settled out, creating vast sedimentary deposits known as the banded iron formations. So all the oxygen produced by cyanobacteria was at first gobbled up by the huge amount of iron dissolved in the seas. Only after most of the dissolved iron in the oceans was depleted could oxygen start to accumulate in the environment, and that is what took 2 billion years - exactly the amount of time that some scientists propose that life was waiting for a fluke event to occur. On the contrary, it seems that the origin of eukaryotes happened as soon as it became possible.

So cyanobacteria were the first to feed the world through modern photosynthesis, they created a crisis that enabled and forced the evolution of aerobic bacteria and the first eukaryotes, and they became the chloroplasts for all eukaryotic algae and plants.  Anything else? Actually, the cyanobacteria probably also invented aerobic respiration itself and passed it on to other bacteria through horizontal gene transfer.

Cyanobacteria had to have a means for protecting themselves from the oxygen they produced, and also for burning the fuel they created through photosynthesis.  They most likely did this at first by running parts of the photosynthetic process backwards.  Look at schematic diagrams of photosynthesis and aerobic respiration.  Though details have changed over time, the two processes are roughly mirror images of each other.  In modern cyanobacteria, photosynthesis and aerobic respiration take place in separate pathways, but these overlap and use some of the same protein complexes.(See Photosynthesis and Respiration in Cyanobacteria, by W. Vermaas)

Stromatolites, like these in Shark Bay, Western Australia, are rare today, but
were abundant in the past.  They are constructed as mats of cyanobacteria
and other microorganisms are laid down one on top of another.  Such
oxygen-rich microenvironments may have been where the first aerobic
bacteria evolved.  Photo by Paul Harrison, posted in
Wikipedia, CC BY-SA 3.0.

The evolution of aerobic bacteria  might have started somewhat earlier than the appearance of oxygen in the open oceans.  Many cyanobacteria lived in peculiar formations called stromatolites, some of which are still around today.  These knobby pillars are formed as cyanobacteria and other microorganisms build sticky mats on their upper surface.  Within these mats, oxygen may have built up locally, creating a microenvironment in which aerobic bacteria may have first evolved. There would be little fossil evidence of such soft-bodied eukaryotes, even after they moved into the open seas.  Our first real evidence of eukaryotes in the fossil record was of algae who had durable cell walls. (see my earlier post on endosymbiosis.)

If all that is not enough to call cyanobacteria superheroes of evolution, there is one more thing.  Whether they invented the process themselves or acquired it from some ancient bacterium through lateral gene transfer, cyanobacteria were and still are major fixers of nitrogen.  This all-important process converts atmospheric nitrogen, which is inert, into ammonia, which organisms can use to make proteins, nucleotides, and countless other essential molecules.  Kudos to the cyanobacteria.

BTW - Much of this is discussed in more detail in my book, Plant Life (if you haven’t read my book yet, why not?!)

References:

Gould, Stephen Jay. 1989. Wonderful Life: The Burgess Shale and the Nature of History. Norton &^ Co

Gribbin, John. 2011. Alone in the Universe - Why our planet is unique. Wiley. NY.

Ward, Peter D and Donald Brownlee. 2000. Rare Earth - Why complex life is uncommon in the universe. Copernicus/ Springer-Verlag. NY.

Conway Morris, Simon. 2015. The runes of evolution: how the universe became self-aware.  Templeton Press. West Conshohoken, PA.

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The first plants

Who were the first plants?   At the risk of a scolding from some of my fellow botanists, I’m going to define plants broadly as organisms that use sunlight to make carbohydrates, and release oxygen gas as a byproduct -   in other words, organisms that photosynthesize.   There is in fact a diverse array of organisms that photosynthesize, including some bacteria and various kinds of algae that are only remotely related to one another; not to mention photosynthetic sea slugs!  So used in that way, "plant" is more of an ecological term for organisms that provide the base of the global food chain, not a precise taxonomic category. (see my post of October 5, 2011, "Plants and animals and kleptoplasts - oh my!")

My goal today is in fact to explore where photosynthesis came from, and we won't be distracted by taxonomic issues.  The first organisms to practice photosynthesis were bacteria, and the cyanobacteria were the first to employ modern photosynthesis, in which oxygen is released as a byproduct.  Bacteria are prokaryotic organisms that have a simple cell structure without nucleus or internal organelles.  They don’t have chloroplasts like true plants or algae, but their entire cell is adapted to conduct photosynthesis.  In my October 5, 2011  post, I described how cyanobacteria in fact were captured and domesticated to become the first chloroplasts.   I also argued as devil’s advocate that cyanobacteria are the only true plants – the multicellular organisms that we call plants are merely the luxury condominiums in which those captured cyanobacteria live!

Cyanobacteria come in many different forms and resemble true eukaryotic algae.  Mat-forming cyanobacteria
 that build stromatolites are similar to to A and B, in which cells are bound by a mucilaginous matrix. on the
surface of a rock.  Drawing from Haupt, Plant Morphology, McGraw-Hill, 1953.

Photosynthesis was invented only once, and passed on to various eukaryotic organisms as chloroplasts, which have been captured, stolen, and recaptured many times.  But when did it all start?  We travel to Australia, where we find some important clues.

In a few shallow, highly saline lagoons along the west coast of Australia, peculiar knobby pillars of rock called stromatolites stand like the disarrayed remnants of a terracotta army, eroded and distorted beyond recognition.  These monoliths were not carved by some ancient civilization, however, but are built up very slowly by microscopic living organisms.   On the tops of the knobs, you can find mats of living microorganisms, held together by a mucilaginous glue.  The glue is secreted primarily by cyanobacteria.  Many bacteria form mats like this.  It’s a good way to anchor yourself to a suitable location.  

Stromatolites at Shark Bay, Western Australia.  Photo by Paul
Harrison via Wikipedia.

Cyanobacteria are massively abundant organisms.  Many live as free-floating plankton or tangles of filaments, and account for as much as 50% of the photosynthesis occurring in open waters (Fig. 2). Others are attached to rocks as filaments or mats.   They are easily confused with true algae, which are eukaryotic organisms with nuclei, chloroplasts, and other organelles.  Before electron microscopy showed us the difference, cyanobacteria were called “blue-green algae.”

Microbial mats on the tops of stromatolites form deposits that extend the knobby pillars slowly upwards.  Particles of sediment and lime precipitated from the water get trapped in the sticky matrix, and periodically bury the living microbes.   The resourceful cyanobacteria in those instances migrate to the top of the sediment and begin a new mat.  This results in a fine structure of alternating light and dark bands.  Stromatolites are thus, like coral reefs, built by the living organisms that inhabit them.   There is a website devoted to Shark Bay in Western Australia (www.sharkbay.org) that includes facts, photos and a video swim through a grove of stromatolites.

             
Stromatolites turn out to be one of our most important clues as to the origin of plant life.  They have been around for about 3.5 million years.  Ancient fossilized stromatolites, which can also be found in parts of Australia, are in fact among the earliest signs of any kind of life on this planet.  They are abundant throughout much of the geological record, but became rather scarce around 500 million years ago.  This was the time of the  “Cambrian Explosion”, when many new kinds of animals appeared.  Stromatolites came under attack by voracious grazing animals equipped with hard, scraping mouth parts.  After that, they survived only in restricted sites too salty for such animals. 

Though there is still debate about whether the earliest stromatolites were formed by cyanobacteria or some earlier form of life, or even by some physical process, there is no doubt that they were building stromatolites  by 2.7 billion years ago – still a heck of a long ago!   Fossilized cells identifiable as cyanobacteria have also been found in slightly different types of rocks, the Warrawoona and Apex cherts of Australia, and these appear also to date back to 3.5 billion years ago.   Cyanobacteria were the plants, the photosynthetic organisms, that supported the Earth’s early ecosystem.  They did so virtually alone form almost 2 billion years, after which the first signs of eukaryotic algae began to appear.

The early photosynthesizers must have gradually built up enormous populations, for the oxygen they produced eventually transformed the vast oceans of our planet, and then the very atmosphere itself.  The scarcity of oxidized (“rusted”) minerals in the Earth’s oldest rocks (older than 3 billion years), indicates that there was very little free oxygen in the atmosphere at that time, so the oxidizing of crustal rocks is also evidence of plant life.  Iron is particularly abundant on Earth, and quite prone to rusting.  In the ancient seas there was a steady supply of iron bubbling up from underwater volcanic fissures, and from eroding surface rocks.  In its unoxidized state, iron is soluble in water, but when it oxidizes it forms insoluble molecules of hematite or magnetite, which sink to the bottom of the sea.  When oxygen became available in comparably huge quantities there were spectacular depositions of iron.  This resulted in distinctive and extensive rock layers known as the Banded Iron Formations.  The “rusting of the earth,” as it was called by Schopf (2006), is the source of most of the iron ore that is being ravenously consumed by modern civilization.

There is some evidence of limited iron formations about 3.5 billion years ago, but they did not become truly massive until the mid-2-billions.   This suggests that oxygen buildup may have occurred sporadically and slowly at first, but became overwhelming between 2.7 and 2.5 billion years ago.  Oxygen makes up 21% of our current atmosphere, but 20 times as much plant-generated oxygen may be tied up in banded iron formations.  The formation of iron deposits declined rapidly after about 2 billion years ago, as the supply of dissolved iron was depleted, and oxygen then began to build up in the atmosphere.   The transformed atmosphere made it possible for more complex organisms to evolve, leading to eukaryotic cells and the modern world of algae, plants, fungi and animals.

So cyanobacteria invented photosynthesis as we know it today, and were the first functional plants.  The story does not end there.  In the two billion years of their unchallenged domination of the Earth, cyanobacteria also invented the rudiments of aerobic respiration and nitrogen-fixation, two other essential metabolic processes - cyanobacteria had to do virtually everything themselves!  Aerobic respiration is the process by  which organisms “burn” carbohydrates to fuel their metabolic processes.  It is obviously essential  for animals, but also for plants.  How else could they  utilize the carbohydrate reserves that they produced for themselves?

In terms of starting ingredients, photosynthesis is easy.  All you  need are carbon dioxide and water, and both are abundant on the planet.  But to make certain other things, like protein, DNA, ATP and other vital organic molecules, you also need nitrogen, which isn’t so easy to come by.  Wait-a-minute, isn’t the Earth’s atmosphere about 70% nitrogen?  Yes, it is, but it’s nitrogen that is hard to use.  Nitrogen gas consists of two nitrogen atoms bound tightly together by a triple bond.  Most organisms can’t break those bonds to make use of the abundant nitrogen supply.  Enter the cyanobacteria.  Somewhere along the way they acquired the genes to split nitrogen, either through mutation and natural selection, or from some other bacterium that invented it first.   Bacteria freely share genes through the process of horizontal gene transfer, a process we exploit in genetic engineering.

Once the nitrogen molecule has been split, cyanobacteria are able to attach hydrogen atoms to the nitrogen, making ammonia, and ammonia then can become the amino group required to make the building blocks of protein – amino acids.  So cyanobacteria, arguably the most successful and certainly the most long-lived group of organisms, make carbohydrates, metabolize carbohydrates for energy, and make their own protein.  The rest of us have only stolen from them!

References:

Schopf, J. W. 2006.  Fossil evidence of Archaean life.  Phil. Trans. R. Soc. B 361: 869–885.

Website for images and more information about stromatolites in Australia: www.sharkbay.org  (under "Nature of Shark Bay")