Introduction

JAAP DEN TOONDER AND PATRICK ONCK

1.1 Natural Cilia

Nature has devised many different ways of creating fluid flow, most of them for animal propulsion, that is, for flying or swimming. At larger scales, examples are the flapping wings of birds, and the waving tails of fishes. Flapping wings are also found at smaller scales in insects. At really small scales, typically for sub-millimetre sizes, a fluid manipulation mechanism used by nature is that by cilia or flagella.

Cilia can be viewed as small hairs or flexible rods, with a typical length between 2 and 15 µm. They cover the outer surface of micro-organisms, such as Paramecia, shown in Figure 1.1a. The length of Paramecia is about 100 µm, and its surface contains over 4000 cilia. These cilia move back and forth in a concerted manner, and are very effective in generating flow: the swimming speed of Paramecium, for example, can be approximately 1 mm s-1 (i.e. it can travel a distance of 10 times its own body length in a second).

An individual cilium moves in a particular, asymmetric manner, as illustrated in Figure 1.1b. It has a so-called effective stroke, during which the cilium is more or less straight, and its effect on the fluid is maximized. During the recovery stroke, its effect on the surrounding fluid is minimized since the cilium has a more curved shape. The micro-organism propulsion is in the direction opposite to the effective stroke. The movement of the cilium is always in a plane perpendicular to the surface during the effective stroke. The recovery stroke movement may lie in the same plane, but also in a plane perpendicular to the effective-stroke plane, so that the movement of a cilium may be truly three-dimensional (the latter is, in fact, the case for Paramecium). The beating frequency of the cilia, typically, is tens of hertz.

The collective movement of the cilia seems to occur in a concerted fashion. Neighbouring cilia move somewhat out of phase, so that a collective wave-like motion, going over the micro-organism's surface, takes place. It is interesting that this wave may travel either in the same direction as the swimming direction of the micro-organism (but opposite to the effective stroke; this is called an antiplectic metachronic wave, and occurs for Paramecium) or in the opposite direction (called symplectic metachronic wave behaviour). This is illustrated in Figure 1.1c. The origin, as well as the physiological reason, for this metachronic co-ordination is not yet completely understood.

Flagella have the same internal structure as cilia, but they are usually longer, typically between 20 and 100 µm, and they do not cover surfaces in large quantities, such as cilia, but as a single flagellum or with a few. Also, their movement is usually different from those of cilia. Instead of having an effective and a recovery stroke, a flagellum mostly makes a helical (cork-skrew) or wave-like motion. The best known example is the flagellum of spermatozoa. A microorganism that is classified as a flagellate by most authors, but as a ciliate by others, is Chlamydomonas (or green algae), shown in Figure 1.2. The length of its body is 10 µm, and it has two flagellates with a length of 10–15 µm. The flagella make an effective recovery stroke, beating with a frequency of about 50 Hz, giving the organism a swimming speed of 100 µm s-1. Interestingly, the beating pattern in Chlamydomonas can change from a typical ciliary beating to flagellar beating upon an external trigger such as intense light or Ca2+.

There are many different micro-organisms that make use of ciliary propulsion or fluid manipulation. Figure 1.3 depicts some of those that can be found in lakes and rivers. Note the scale bar on the right, representing a length of 1 mm.

Next to active cilia, which are used to induce movement, cilia are also used for sensing, for example of fluid flow, but also for detecting other physical and chemical signals. Both motile and non-motile cilia and flagella are present in the human body, at various locations and with various functions, as shown in Figure 1.4. For example, there are cilia in the cochlear, the inner ear, that contribute in detection of vibration caused by sound. As already mentioned, each spermatozoon swims by beating a flagellum. Also, the Fallopian tubes of females are covered with cilia that move the fertilized ovum from the ovary to the uterus, where the ovum attaches itself. Motile cilia are also present in the lining of human lungs and the windpipe (trachea), to sweep mucus and dirt out of the airways in order to avoid infections. More examples of cilia within the human body can be found in Ibanez-Tallon et al.

Motile cilia and flagella both have the same characteristic internal structure. The skeleton of a cilium (or flagella) is made up by a flexible cylindrical structure that is called the axoneme. Figure 1.5a schematically depicts the constituents of the axoneme, showing the structure that is so characteristic for all motile cilia and flagella. An electron micrograph of the cross section of a cilium can be seen in Figure 1.5b. Nine pairs of micro-tubules are arranged along the periphery, and one pair of micro-tubules is situated at the centre. Micro-tubules are biopolymer filaments, which, for example, can also be found in the cytoskeleton (the internal skeleton of cells). They are hollow rods approximately 25 nm in outer diameter and 14 nm inner diameter. For obvious reasons, the axoneme structure shown is known as the 9 + 2 axoneme.

The nine outer pairs of micro-tubules are connected by nexin links. Also, each of the outer pairs is linked to the central pair by a radial spoke. A closer inspection of the...