An ode to sponges, skeletons and bacteria

Sponges are not what you’d normally think of as “exciting” animals. They are simple creatures that spend the entirety of their adult lives sitting around, patiently sifting immense amounts of water for microscopic food. The closest most of them get to “doing” anything is popping out a few babies every now and then. (Exception: deadly shrimp-killin’ predators :o) However, these (mostly) placid filter feeders have a lot to offer once we move past the usual coolness filters that make our inner ten-year-old a Velociraptor fan*.

I’ve been getting quite fond of sponges recently. It’s mostly a byproduct of the reading I do for my work, which partly concerns the mineralised hard parts of animals. All sponges have skeletons, and the majority of them make hard(ish) skeletons from one of two minerals: either amorphous silica (think glass) or calcium carbonate (think chalk, limestone, clam shell, etc.) (The rest, including bath sponges, use proteins.) Siliceous sponges in the class Hexactinellida (= glass sponges proper) can have beautiful, intricate skeletons like this one from a Venus’s flower basket (Euplectella sp. by NEON ja, Wikimedia Commons):

They are not only gorgeous, but, at least in some cases, also insanely strong and bendy – nature’s fibreglass fishing rods, if you like. See this photo from sponge guru Werner Müller’s group for a demonstration. That glass rod is the skeleton of Monorhaphis chuni, a deep-sea glass sponge that anchors itself with the largest known single structure made of silica in the living world. This “giant spicule” can be up to 3 m long, and flexible enough to bend around in a circle (Levi et al., 1989).

Some sponges have both glassy and calcareous (or “chalky”, if you like) skeletons. And such sponges are giving me all kinds of squee moments lately. Something I’ve only learned recently is that sponges often live in close association with a variety of bacteria. Now it turns out that these symbiotic bacteria contribute to their skeleton-building abilities!

Last year, Dan Jackson and his team published evidence that a sponge species stole a gene it uses to make its calcareous skeleton from a bacterium (Jackson et al., 2011). The gene in question occurs only in bacteria – and sponges. While the sponge species used in the study does harbour bacteria in the cells that produce the calcareous portion of its skeleton, multiple lines of evidence indicate that the gene in question sits in its own genome, and has done so for a long time. It is only active in the skeleton-forming cells, and its protein product is present in bits of skeleton isolated from the animal, suggesting that it does in fact function in building the skeleton. (As of that study, its exact role is still unknown.)

(Above: Astrosclera willeyana, coralline sponge and convicted gene thief. The living animal forms a crust over an ever-growing bulk of dead skeleton. From Jackson et al. [2011])

Most recently, another “spongy” research team found that members of a different sponge lineage have the actual bacteria in their cells make their skeletons for them. Uriz et al. (2012) examined three species of crater sponges, belonging to the “siliceous” sponge genus Hemimycale. In certain cells of the animals, they saw tiny round objects that molecular genetic tests revealed to be bacteria. The bacterial cells were surrounded by a coat of varying thickness that, when the researchers probed its elemental composition using X-rays, proved to be made of calcium carbonate. According to their observations, the bacteria live and divide inside membrane-enclosed vacuoles. They accumulate calcareous material as they mature, and finally the host cell spits them out to form a mineral crust around the animal. (Below: colonies of Hemimycale columella, one of the three species used in the study, from the Encyclopedia of Marine Life of Britain and Ireland via Encyclopedia of Life)

The bacteria look like they’ve had a long-standing partnership with their host sponges. They were abundant in all examined individuals of all three species. Unlike free-living bacteria, they appear to lack cell walls. They are also inherited by baby sponges. Mother Hemimycale sponges nurture their embryos in their bodies (apparently this is common among sponges). Sponges provide their embryos with so-called nurse cells, which, in the case of these species, contain some mineral-making bacteria. The young sponge eventually eats the nurse cells, thereby acquiring the bacteria. By the time it becomes independent and settles on a comfortable rock, its body is littered with tiny mineral spheres made by its inherited symbionts.

On closer examination, it seems that Hemimycale is far from the only sponge genus to harbour similar hired skeleton-builders. Uriz and colleagues tell us that they have found previously overlooked evidence of such “calcibacteria” in several other sponges – one of which is only distantly related to Hemimycale. Could calcibacteria be ancient partners of these animals, inherited by many different sponges from a distant common ancestor? Could bacteria even hold the key to the origin of calcareous animal skeletons?

(FWIW, I don’t really buy the second idea. As far as I know, all non-sponge animals that have been investigated make their skeletons with their own genes – nothing suspiciously bacterial-like the way Jackson et al.‘s spherulin is. [Caveat: there remain plenty of groups that haven’t been investigated in sufficient molecular detail.] However, the idea that sponges as a whole may have acquired their calcareous skeletons this way is fascinating. Incidentally, though the ID isn’t 100% certain yet, the calcibacteria may belong to the same bacterial class as mitochondria and these insidious bastards. Do alpha-proteobacteria have a special knack for endosymbiosis?)

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*Not to say Velociraptor isn’t cool, but being a vicious toothed, raptor-clawed killer bird is, well, not the only road to coolness 😛

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ETA: 42nd post, yay! (Also yay: random Hitchhiker’s Guide reference in completely unrelated post :D)

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References:

Jackson DJ et al. (2011) A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy. BMC Evolutionary Biology 11:238

Levi C et al. (1989) A remarkably strong natural glassy rod: the anchoring spicule of theMonorhaphis sponge. Journal of Materials Science Letters 8:337-339

Uriz MJ et al. (2012) Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in Metazoa? Evolution early online view, doi: 10.1111/j.1558-5646.2012.01676.x

Much ado about nothing

I am disappointed.

I have a soft spot for Kimberella, one of the few Precambrian animals that we can identify with reasonable precision. (Not to mention its pretty name! :D) Our love affair started before I became involved with biomineralisation, which might have contributed to the fact that I totally overlooked Ivantsov (2009).

(Image: Ivantsov’s Kimberella, rendered by the masterful hands of Nobu Tamura. From Wikipedia.)

The paper shows up on Kimberella‘s lovely Wikipedia page as a citation for the following:

The deformation observed in elongated and folded specimens illustrates that the shell was highly malleable; perhaps, rather than a single integument, it consisted of an aggregation of (mineralized?) sclerites.

These days when I’m >this< close to dreaming about biominerals at night, this jumped out at me like a giant neon sign. What? A mineralising animal that old? (I think this was also before I saw Coronacollina.) So I downloaded the paper, and eventually got round to reading it, and…

Pfft.

It’s an alright piece of scientific literature, and it’s got lots of lovely pictures of Kimberella fossils (though Fedonkin et al. [2007] already had a ton of those). I would have been happy about it but for the fact that it totally flopped on the mineral thing. I thought that, you know, Ivantsov had some evidence to suggest that those bumps on the creature’s back were originally made of mineral stuff. And, indeed, his abstract quite confidently states not only that they were mineralised but also the specific mineral:

The fossil material shows that Kimberella had hard sclerites, probably of aragonite…

His reasoning? Let me quote…

The alternation of nodes and coarse folds in the central zone of the fossil may be explained by assuming that the nuclei of nodes were clumps of hard substance, which rapidly destroyed after the death of the animal. Aragonite, which obviously had no chances to be preserved in the terrigenous sediment, which, in addition, was saturated with hydrogen sulfide (Gehling, 2005), could have been such a substance.

I mean, really? They “could have been” made of aragonite because they disappeared? It’s like there is no other tough-ish material that can be destroyed after an animal dies. And he doesn’t go any deeper than that – no discussing/excluding other possibilities, nothing. He just leaves it there.

People, can you please not claim things in your abstracts that you then barely discuss, let alone demonstrate, in the paper?

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References:

Fedonkin MA et al. (2007) New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. In: Vickers-Rich P & Komarower P (eds). The Rise and Fall of the Ediacaran Biota. Geological Society, London, Special Publications 286:157-179

Ivantsov YA (2009) New reconstruction of Kimberella, problematic Vendian metazoan. Paleontological Journal 43:601-611

News bites

Just quickly before I completely forget about these…

(1) Common ancestry of segmentation: back-and-forth-and-back-and-forth

Seaver EC et al.(2012) Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation. EvoDevo 3:8

I’ve made throwaway mentions of segmentation before. The conundrum about segmentation is whether (or rather, to what extent) it is homologous in the three “eusegmented” phyla, arthropods, annelids and chordates. It arises because all three phyla are separated from the others by many lineages that aren’t usually considered segmented – yet the three share some tantalising similarities. People have been trying to solve the question by comparing the genetic mechanisms generating the segments in each group, with mixed results. One of the papers in my previous news bite post was about the similarity of segmentation in arthropods and vertebrates. Now, here’s one for the differences between arthropods and the wormies. (You can’t say I’m not fair :-P) The genes listed in the study’s title were originally described in the fruit fly Drosophila melanogaster, one of the best studied animals in developmental biology (and, like, every other area of biology). There, they have an interesting role in that each of them helps define every other body segment. IIRC, Pax3/7 (known in flies as paired) and even-skipped are for even-numbered segments, runt is for the odd ones. Now, segmentation in Drosophila is (to put it mildly) fucking weird, but if memory serves, several of these pair-rule genes have been confirmed to play similar roles in less eccentric arthropods. Elaine Seaver and colleagues looked at their expression in their favourite worm (this guy. Seaver’s group obviously didn’t pick it for its beauty :-P), and they found that they were active in… nothing resembling a two-segment pattern. Or anything segment-related. The more genetic studies come out, the more complicated the whole segmentation issue is looking…

(2) Someone found the cause of the Cambrian explosion. (Again.)

Peters SE & Gaines RR (2012) Formation of the ‘Great Unconformity’ as a trigger for the Cambrian explosion. Nature 484:363-366

The Cambrian explosion is probably not what you think it is (no, all animal phyla didn’t just suddenly pop into existence fully formed ;)). Nevertheless, the (relatively) quick rise of animals – particularly animals with hard parts – beginning in the Early Cambrian is still odd enough to fascinate generations of palaeontologists, evolutionary biologists and geologists. The list of proposed causes is pretty long by this point (and believe me, I really really would like to go into them once… but, uh. Huge, dauntingly huge topic). Explanations range from denying the need for an explanation through pinning it on oxygen levels, ice ages, developmental genetics, predation, biomineralisation, even the evolution of eyes, and, working from memory, I probably left some more out of that list. Peters and Gaines’ preferred explanation seems to be geological and ecological: they suggest that a combination of lots of erosion/weathering on land, and a subsequent rise in sea levels, led to large new shallow seas that were chock full of dissolved minerals. New habitats to conquer + widely available minerals = an explosion of new animals with mineralised hard parts. This study is a nice two-in-one: it purports to explain not only the Cambrian explosion, but also the conspicuous gap in the geological record that separates Cambrian from Precambrian rocks in many places.

Back to the warm little pond?

Oh, look, an abiogenesis post again! This time, of pure squee.

Back in olden days, a certain Charles Darwin wrote to a dear friend:

“It is often said that all the conditions for the first production of a living organism are now present, which could ever have been present. But if (and oh! what a big if!) we could conceive in some warm little pond, with all sorts of ammonia and phosphoric salts, light, heat, electricity, &c., present, that a proteine compound was chemically formed ready to undergo stillmore complex changes, at the present day such matter would be instantly devoured or absorbed, which would not have been the case before living creatures were formed.”

The famous quote is obviously not a theory of abiogenesis as such; rather, it’s some (fairly obvious, in hindsight) reasoning as to why life doesn’t originate anew today. Still, the warm little pond has become something of a symbol for abiogenesis.

Ironically, it doesn’t seem to enjoy much popularity in the field itself.* The scientist favourites are more along volcanic lines – hydrothermal vents of some stripe, or cold seeps on the seafloor. The sea is a common theme with these… but volcanic environments spewing all kinds of useful chemicals are not limited to the sea. In fact, Mulkidjanian et al. (2012) argue, much more abiogenesis-friendly volcanic sites might be found on dry land.

Living cells, the reasoning goes, contain far higher concentrations of potassium, phosphate, zinc and some other ions than any ocean anywhere (and, most likely, anytime) on the planet. The most ancient proteins that are still present in living things today don’t simply tolerate these ions – they depend on them. However, the first cells would not yet have possessed the tightly insulating membranes and armada of ion-shuttling proteins modern cells use to maintain their special salt cocktail in all kinds of environments. Therefore, cells must have arisen in a salt solution similar to their interiors. (Note that this reasoning doesn’t necessarily apply to the origin of replicating molecules. We’re not talking about the very first steps towards life just yet.)

Where might one find such an environment? Not anywhere in the sea, the researchers argue. “[H]igh concentrations of transition metals, such as [zinc] and [manganese], are found only where extremely hot hydrothermal fluids leach metal ions from the crust and bring them to the surface,” they remind (pE823). Now, this also happens at deep sea vent systems – but deep sea vents don’t spill out much phosphate, so they only contain part of the “life cocktail”. Geothermal fields on land, on the other hand… Geothermal regions where the hot water boils and steams through the rock are also potassium-rich (again, unlike any place in the sea), bringing all the essential ingredients together. The steam either boils all the way to the surface and then condenses in pools, or reach the surface as a liquid and result in nice, bubbling mud pots.

These environments today are very acidic, which is not generally good for life – however, their acidity is the result of hydrogen sulphide reacting with oxygen. There was very little oxygen in the ancient atmosphere, so the first protocells forming in a primordial mud pot or hot volcanic pool wouldn’t have to contend with that little nuisance called sulphuric acid. What’s more, the silica carried by the rising steam would precipitate as silicate minerals of the exact sort that are thought to be conducive to the formation of all kinds of protocelly things including primordial lipid membranes and nucleic acids (Hanczyc et al., 2003)!

Swell! And there are other little gems scattered throughout Mulkidjanian et al. (2012). For example, some of the minerals that form in a geothermal environment without oxygen can catalyse the formation of various organic compounds, which the early protocells could eat. Inland geothermal fields also live much longer than deep sea vents, providing more time for life to get off the ground. What’s more, the rocks wetted by condensing geothermal vapours would dry out and then be re-wetted many times, which concentrates some of the organic chemicals thought to be most important for the origin of key life molecules like nucleic acids. Even better, geothermal vapours are full of borate, which can stabilise ribose – a component of RNA, thought to be the substance of the first genomes.

So, this study envisions a field of geysers, mud pots and warm pools fed by the runoff as the cradle of life. Probably not quite what Darwin had in mind, but hey, when Darwin thought up his warm little pond, people thought proteins were the substance of inheritance. I think we can give him a little slack here 😉

We’ll see what other abiogenesis researchers have to say about the idea, but for the time being, I rather like it!

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*Disclaimer: my reading on abiogenesis mostly consists of fangirling over interesting new ribozymes and cdk007’s Youtube videos. It’s not a field I would call myself well-versed in. So what “seems” to me might just be a nosy outsider’s distorted impression 😛 (Nonetheless, the paper seems to express the same impression, and the authors ain’t newbies to this field. Well, Eugene Koonin, the principal investigator, certainly isn’t.)

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References:

Darwin’s letter to Joseph Hooker is recorded in Darwin F (ed.) (1887) The life and letters of Charles Darwin, including an autobiographical chapter. London: John Murray. Volume 3.

Hanczyc MM et al. (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618-622

Mulkidjanian AY et al. (2012) Origin of the first cells at terrestrial, anoxic geothermal fields. PNAS 109:E821-E830