How Hydra Eats

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Sheets of epithelial cells allow animal tissues to define inside and outside, and as such are arguably the fundamental building block of metazoan life. Because of this topological role, the folding, stretching, and on occasion disruption of epithelial sheets is a central feature of both embryonic development and tissue regeneration. In this study, Carter et al. (1) examine a particularly intriguing example of epithelial gymnastics, mouth opening in the freshwater polyp, Hydra vulgaris.

Hydra are millimeter-sized animals from the same phylum as jellyfish, Cnidaria. They have long fascinated biologists due to their ability to regenerate after injury. Remarkably, even cells from a mechanically dissociated Hydra can reaggregate, and over the course of about a week reassemble into a functioning animal (2). How this process occurs remains poorly understood, but points to a remarkable degree of potential plasticity in metazoan tissues that is largely lost in organisms such as ourselves.

In this study, Carter et al. (1) examined a simpler problem, namely how Hydra open their mouths. The authors show that mouth opening is controlled by radial and circumferential myonemes, contractile cell bundles that function in a manner similar to the muscles that control the diameter of the eye’s pupil. Remarkably, the Hydra mouth is not a permanent opening (Fig. 1). Instead, when the mouth is closed it is sealed by a continuous epithelial sheet (3). For the mouth to open this sheet must be disrupted, introducing a hole that expands in <1 min to a diameter that can be larger than the animal’s body. How exactly this rapid expansion occurs has been unclear. Large-scale tissue rearrangements in other systems—for example, Drosophila germ band extension—are driven by the rearrangements of cell-cell contacts (4, 5). However, Hydra’s mouth opens much faster than typical developmental timescales, suggesting that cellular rearrangements would need to be very fast if they indeed occur.

Figure 1.

A Hydra, with the ectoderm in green and the endoderm in purple. In this image the mouth is closed. The mouth forms at the center of the apical (top) surface between the tentacles. Scale bar is 50 μm. Figure provided by E.M.S. Collins. To see this figure in color, go online.

To address this puzzle, Carter et al. (1) took advantage of transgenic Hydra, which have become available only relatively recently, to directly track the movements of individual cells in the animal’s ectoderm and endoderm as the mouth opened. By tracking individual cells, the authors were able to conclude that cell-cell junctions do not rearrange: instead, cells near the border of the mouth stretch, sometimes dramatically, to accommodate the change in tissue shape.

Further analysis allowed Carter et al. (1) to propose a reasonable physical model to describe how mouth opening may occur. In a separate set of experiments, they determined the elastic moduli of the tissues making up the mouth to be ∼5 kPa, a value that is reasonably consistent with other simple epithelia (6, 7). Using this value, plus the relaxation time associated with mouth opening, the authors could estimate an effective tissue viscosity of ∼4 × 10⁴ Pa·s, a value consistent with those measured for zebrafish embryonic tissues (8). Simplifying assumptions allowed the authors to estimate the overall forces that lead to mouth opening at ∼1–2 nN, similar to the force necessary to rupture tight junctions between neighboring mammalian epithelial cells (9). The overall picture is that the radial myonemes generate sufficient force to break a few cell-cell junctions at the center of the mouth pore, but not so much as to rip the tissue apart. Mouth opening stops when the restoring force of the stretched tissue counterbalances the force generated by myoneme contraction.

The evolutionary advantages of Hydra’s mouth opening mechanism are, at least at present, unclear. Reasonably closely related Cnidaria possess permanent mouths, showing that there is in principle no evolutionary barrier to Hydra using a more conventional eating arrangement (3). It is plausible that the small size of Hydra makes their unusual (by our standards) method of eating feasible. The measurements of Carter et al. (1) show that individual cells undergo >100% strains during mouth opening. Presumably, larger Hydra-style mouths would either require even larger strains that could threaten the tissue integrity, or alternately require cellular rearrangement, which at least in familiar examples is slow. The minimalist mechanism uncovered here is evidently sufficient for Hydra’s needs.

What is the use of understanding how Hydra, an inoffensive creature of negligible economic value, opens its mouth? As Yogi Berra said, “You can observe a lot by watching.” This study is notable in its use of simple, elegant measurements and modeling to derive insight into an ostensibly complex tissue movement. This and other conceptually related studies offer solid grounds to believe that tissue morphogenesis, which at first blush might seem hopelessly complex, can in fact be understood using relatively simple physics (10, 11, 12).

Relatedly, this study illustrates the benefits of expanding our repertoire of biological model systems to encompass the marvelous diversity presented by the tree of life. Nonstandard model organisms such as Hydra, Ciona, Trichoplax, and more broadly the vast array of creatures that cohabit our planet present evolutionary experiments, in which biological truths obscured by the idiosyncrasies of standard model organisms may be readily discerned (13, 14, 15, 16). Further, rapid improvements in genome sequencing and genetic manipulation are opening up new classes of organisms to sophisticated experiments that until recently could only be accomplished in a few species. The work by Carter et al. (1) provides a useful example of how to adapt neglected organisms to quantitative, biophysical research, and nicely illustrates the fruits of doing so.

Editor: Jennifer Curtis