Doushantuo embryos dethroned?

Almost ten years ago, there was a spectacular fossil discovery in China: microfossils, tiny organisms preserved by phosphatization, that revealed amazing levels of fine detail. These specimens were identified as early animal embryos on the basis of a number of properties.

  • The cells were dimpled and shaped by adjoining cells, suggesting a flexible membrane—not a cell wall. This rules out algae, fungi, and plants.
  • The number of cells within each specimen was usually a power of 2. This is something we typically see in cleaving embryos, the sequence from 1 to 2 to 4 to 8 to 16 cells.
  • They were big. Typical somatic cells in animals are 5-10 µm in diameter, but ova can be a millimeter or more in diameter, and individual blastomeres (the cells in the cleavage stage embryo) can be several hundred µm across. These cells and the whole assemblage were in that size range.
  • The individual cells were uniform in size, as seen in many cleavage stage embryos, and contained organelles arranged in a consistent pattern.
  • They were often found encapsulated in a thin membrane, similar to the protective membrane around embryos.

There are some concerns about the interpretation, though. One troubling aspect of their distribution is that they are all only in the cleavage stage: we don’t see any gastrulas, the stage at which embryonic cells undergo shape changes and begin to move in a specific, directed manner. Studies of taphonomy (analyses of the processes that lead to fossilization) have shown that these later stages are particularly difficult to preserve, which potentially explains why we’re seeing a biased sample. Another unusual bias in the sample is that all of the embryos exhibit that regularity of division that produces equal-sized blastomeres—yet many invertebrate embryos have early asymmetric cleavages that produce recognizable, stereotyped distributions of cells. That asymmetry could be a feature that evolved late, but at the same time, some of the fossils were described as resembling molluscan trefoil embryos. Why aren’t the examples of early asymmetry translated into a later asymmetry?

Now there’s another reason to question the identity of the Doushantuo microfossils: they may be bacterial.

Bailey et al. have pointed out some stunning similarities between the phosphatized Doushantuo microfossils and sulfur-oxidizing bacteria of the genus Thiomargarita. They are of approximately the same size, form colonies of uniformly sized individuals that are the product of cell division and are in numbers that are powers of two, and now, suddenly, it seems that quite a few of the parameters of the fossils that were thought to be diagnostic of an animal embryo are much more ambiguous. Look for yourself: Thiomargarita is in the left column, representative microfossils on the right.

a, Solitary Thiomargarita cell from the Gulf of Mexico (after ref. 2). b, Two-cell cluster of Thiomargarita. c, Three-cell Thiomargarita cluster, thought to result from the incomplete division of a two-cell cluster. Greek letters identify each of the three cells. d, Tetragonal Thiomargarita tetrad resulting from reductive division in two planes. e, Offset between opposing cells in rhomboidal Thiomargarita tetrads resembles offset in some Doushantuo tetrads and cross-furrows in four-cell blastulas. Arrows indicate thin sheath surrounding cell cluster. a’, Megasphaera inornata, from the Doushantuo Formation. b’, Two appressed hemispherical bodies enclosed by an external envelope. c’, Thiomargarita triplets occasionally result from incomplete division, which results in two cells with a combined volume roughly equal to the third undivided cell. This Doushantuo globular triplet shows similar relative volumes. d’, Parapandorina tetrad resulting from division in two planes. e’, Doushantuo rhomboidal tetrad. Scale bars, 150 µm (b’); 100 µm (a?e, a’, c’?e’).

It doesn’t disprove their identification as embryos, but it does provide a strong alternative explanation that we will have to consider in any interpretation. In addition, these sulfur-oxidizing bacteria promote chemical reactions that can precipitate phosphates, generating the very conditions that preserve them so well. These conditions would also help preserve other organisms in the neighborhood, so it could be the case that what we’re seeing is a cloud of large bacteria that make a matrix that preserves other organisms—like, perhaps, some embryos.

As I’ve said before, I love the idea of being able to see 580 million year old embryos. Should I be disappointed at learning that perhaps these fossils are not of embryos?

Why, no.

I like reality and evidence. If further data demonstrate that not one of these fossils is a metazoan embryo and that all of them are interesting and unusual examples of large, specialized bacteria, that will be cool in a different sort of way. We follow where the evidence leads us, not where our predispositions want us to go.

Besides, there is one other fascinating part of this alternative explanation. The idea that the morphology of assemblages of bacteria might be superficially indistinguishable from the attributes of early metazoan embryos further blurs the line between the single-celled and multicellular worlds—the transition becomes even less difficult to explain. The basic principles of early development are not unique or miraculous or abrupt, they are extensions of molecular strategies pioneered in bacteria.

Bailey JV, Joye SB, Kalanetra KM, Flood BE, Corsetti FA (2006) Evidence of giant sulphur bacteria in Neoproterozoic phosphorites.
Nature advance online publication 20 December 2006.