Bacteria invented multicellularity – then thought better of it

I get content alerts from a whole host of journals, some specialist publications focusing on my field, some more general. The majority of even the former is stuff I couldn’t care less about, and the ratio of interesting to irrelevant from generalist journals like PNAS or Nature is lower still. Nevertheless, sometimes you stumble on a title that isn’t directly related to your main interests, but still makes the whole rummaging through the Pile of Irrelevance worth it.

This was the case with a paper (Schirrmeister et al., 2011) just published in the online, open-access journal BMC Evolutionary Biology. It’s so fresh that they haven’t even formatted it – the full text is only available as a “provisional” pdf where all the figures are dumped at the back of the file, separated from their captions (why they can’t wait with publication until the damned thing is in readable format escapes me).

The study by Schirrmeister and others deals with an unusual group of bacteria. Cyanobacteria are probably still better known as blue-green algae, even though they have nothing to do with anything else we call an alga (well, in truth they have everything to do with algae, but in a rather more interesting way, as we’ll see below). If I had to pick one group of organisms that had the greatest impact on the history of our planet, cyanobacteria would be it. For more than two billion years, they have contributed huge amounts of biomass to the global carbon cycle. They are solely responsible for the oxygen-rich atmosphere of the earth – and, by extension, for most eukaryotic life and all animals. They are among the distinguished group of bacteria that can fix nitrogen – a vital ingredient of DNA and proteins – straight from the air, making it available for other organisms. Without them, the world would be a vastly different place, and we wouldn’t be possible. As Andrew Knoll puts it in his wonderful book Life on a Young Planet (consider this a recommendation ;)): “animals may be evolution’s icing, but bacteria are the cake”.

Cyanobacteria live everywhere there is light, from hot springs to the ocean to puddles to stone walls (as components of lichens). They also live inside the cells of every single eukaryote capable of photosynthesis: plants, red and green algae, brown algae, diatoms, dinoflagellates, euglenids (and any others I forgot to mention). The chloroplast is a pared down cyanobacterium – a symbiont that has lost most of its genes, but the ones that remain, together with its structure, still tell of its ancestry. Plants owe all their green splendour to these tiny buggers.

Cyanobacteria are not just immensely important, they are also quite unusual among prokaryotes. As the post title implies, they invented multicellularity. Multicellular cyanobacteria display a range of complexity. Some of them are just chains of identical cells. Others, though, have up to three different cell types. Heterocysts, thick-walled cells that ensure the oxygen-free environment that these bacteria require for nitrogen fixation, sit at regular intervals among “normal” cells, and when necessary, the “normal” cells can also differentiate into hardy resting cells that can survive bad times. The most complex cyanobacteria not only have filaments with different cell types, but also introduce branching into these filaments. This is the most complex prokaryotes get.

Filaments of an unbranched, differentiated cyanobacterium. The oversized heterocysts are quite obvious in some of them. Image by Kristian Peters, from Wikimedia Commons.

The new study raises an interesting possibility: that at least the simple form of multicellularity (i.e. undifferentiated filaments) occurred very early in the history of cyanobacteria. According to Schirrmeister et al., the vast majority of modern cyanobacteria descend from multicellular ancestors, even though a great many of them are single-celled today. Even more intriguingly, they find a lineage that might have re-evolved multicellularity after losing it. I don’t pretend to fully understand the methods used to come to these conclusions, but I have to say that it’s built on an impressive dataset – the group selected 58 cyanobacterial species for more detailed study from an original phylogenetic tree built from over a thousand taxa. They then constructed trees of this smaller dataset using two separate methods, and finally, tried to reconstruct the ancestral states at various points in those trees using several different statistical methods again. The analyses all agree: multicellularity is a very ancient trait in cyanobacteria, and it was lost left and right during their three-billion-year history.

These findings go against our ingrained view of evolution as an inexorable march towards increasing complexity. We, mammals, are among the (if not the) most complex organisms the earth has ever produced. We are assemblages of some 200 distinct cell types organised into a finely regulated machinery of a multitude of specialised organs. When we look at the large-scale patterns in the fossil record, we also see that this complexity has accumulated from much simpler beginnings over the aeons. We can be forgiven for thinking, in a characteristically self-centred way, that complexity is where evolution is intrinsically headed. But every now and then, nature reminds us that “more complicated” does not necessarily equal “favoured”.

Parasites are probably best known for their tendency to become simplified – after all, if you are bathed in your host’s digestion products all the time, why waste your energy on growing your own gut? However, simplification is abundant in organisms that make their own living, too. For example, two entire phyla of distinctly unsegmented, baglike worms – spoon worms and peanut worms -, likely came from more sophisticated segmented worms (Struck et al., 2007). Now, cyanobacteria join the club, and new questions surge in their wake. Why did they go back to unicellularity? How difficult is it for them to become multicellular? Such questions, of course, can be asked about any complex trait that followed a similar evolutionary trajectory.

Most intriguingly, these tiny microbes seem to violate another “law” of evolution, known as Dollo’s law: that once lost in a lineage, a complex trait won’t reappear. If the inferences of Schirrmeister et al. are correct, then either simple multicellularity isn’t such a big deal at all for these bacteria, or Dollo’s law isn’t as much of a law as we thought.

(Actually, the latter is probably the case however the history of cyanobacteria turns out. Dollo’s law has been questioned by others, and it was recently dealt a spectacular blow by a frog that almost certainly re-evolved teeth in its lower jaw (Wiens, 2011) after at least 200 million years of not having them.)

Evolution is a fascinating story. As the example of cyanobacterial multicellularity suggests, it can also be as complex as any good novel. I for one think this makes for a much more interesting and fulfilling narrative than simplistic listings of “what’s new” through the ages.

– – –

References:

Schirrmeister BE, Antonelli A and Bagheri HC (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11:45

Struck TH et al. (2007) Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7:57

Wiens JJ (2011) Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluation of Dollo’s Law. Evolution advance online publication, DOI: 10.1111/j.1558-5646.2011.01221.x

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