Why would a strict intracellular organism be motile? In the case of rickettsiae (and some not strict intracellular parasites such as the listeriae and shigellae), motility is carried out through the activity of the host's actin, apparently for the purpose of infecting adjacent cells. I am not talking about that, but rather I will consider here the intrinsic motility of those exemplars of intracellularity, the chlamydiae and the rickettsiae. Why would they sprout flagella and move around, possibly extracellularly? But before I will deal with this puzzle, I want to introduce aspects of the chlamydiae, a group of organisms that I find particularly attention-grabbing.
About the Chlamydiae
Everybody, especially college students, know about the chlamydiae for their ability to cause the most common sexually-transmitted disease in the US and elsewhere. But there is much more to this group of organisms, something that is not always known to many microbiologists either. It turns out that chlamydiae are nearly ubiquitous, being found within a large variety of animals and plants. Included are vertebrates, such as people or the leafy sea-dragon and the barramundi, invertebrates like the sweet potato whitefly, and many protists. Free-living amoebas are frequent hosts for chlamydiae and their ilk, which are the best studied of the environmental chlamydiae. In addition, chlamydial rRNA sequences have been found in a remarkable variety of habitats, such as soils, sediments, hydrothermal vents, sludge, plus, plus. In other words, they seem to be everywhere. They are surely underappreciated, despite some of environmental strains apparently being able to infect humans. (Proving Koch's postulate here as elsewhere is not always easy). One species, Chlamydophila pneumoniae, is said not only to cause pneumonia but also to be associated – in ways as yet uncertain – with atherosclerosis, asthma, and Alzheimer's disease no less.
Chlamydiae undergo a rather complex life cycle that comprises a tough, environmentally resistant stage called 'Elementary Body' and a reproductive one, known as 'Reticulate Body.' The morphology of these developmental stages varies considerably with the species, from rod- to crescent- to star-shaped. Inside host cells, these forms tend to live in clumps known as 'Inclusion Bodies,' which are readily visible in pathological specimens. What else? Chlamydiae tend to have small genomes, about 1 Mb in size, and to lack the genes for amino acid biosynthesis and for making some nucleotides. They have ADP/ATP translocases that allow them to import these energy rich compounds. Phylogenetics suggest that they have been strict intracellular parasites since their early days.
Did Chlamydiae Help Plants Evolve?
Recent work on this group of organisms has revealed a whole lot of interesting things about them but perhaps the main one is that they have played a key role in the origin of plants. This curious inference arises from chlamydial proteins being remarkably like those of cyanobacteria and plants and, even more surprising, being able to function in plastids. In one species, over 150 proteins have high sequence similarity to those of cyanobacteria and plants. In addition, some of the chlamydiae have a 23S rRNA intron, which are characteristic of algal plastids, archaea, and lower eukaryotes, but absent from most bacteria. So, what happened here? Hypotheses abound, but perhaps the most credible one at present is that chlamydia participated in a tripartite affair, along with the ur-eukaryote and the bacteria that became mitochondria and plastids. The work of Hueng and Gogarten supports this possibility. They found that 21 genes were transferred between chlamydiae, a red alga and plants. They and others (see for example here and here) proposed that the chlamydiae worked to help the future plastid (a cyanobacterium) become established in the plant. This has been called the MAT (for Ménage á Trois) hypothesis, although the way it worked has not been fully worked out. Not surprisingly, this daring notion has been forcefully contested.
Are Chlamydiae Motile?
Now for the gist of this post. A recent paper presents data for some marine chlamydiae possessing genes for a complete flagellar apparatus, just like that of free-living bacteria. How was this revealed? The authors sequenced three genomes from single cells in samples from three marine sites from the Pacific and Atlantic oceans. They are distinct from other chlamydiae and probably represent deep branches within the phylum. In these genomes, the researchers were surprised to find 5 examples in one sample and 20 in the others of genes that match those of bacterial flagella. Included are those for all the cytoplasmic, transmembrane, and extracellular components. These genes appear to be of ancient origin and not to have been acquired by recent horizontal transfer. However, they are phylogenetically distinct from those of other bacteria. So, what are these genes for? Do chlamydiae actively move about, perhaps chemotactically?
The researchers looked for genes involved in chemotaxis and indeed found them in all three samples. Given that chlamydiae have reduced genomes, finding such sets of genes suggest that they are required for survival in these organisms. Is it possible that these organisms, even if incapable of reproducing outside of host cells, are able to move about in the environment? The reason could be that if you are motile you may have an easier time finding new hosts. The energy requirement in the transit forms (elementary bodies) could be stored in the glycogen they carry. This contradicts the generally held view that extracellular chlamydiae are metabolically inert. Most of them may be. But a few, perhaps just marine ones, may use motility gene products to adhere to particles, to act as sensors or to function as part secretion systems. Keep in mind that bacterial flagella are involved in many functions. This aspect of chlamydial biology clearly awaits retrieving the organisms, not just their genomes.
Should We Redefine Strict Intracellular Parasitism?
Surprising as the finding of possible chlamydial motility may be, it is not unique. The other major group of strict intracellular bacteria, the rickettsiae, not only have flagellar genes but carry actual honest-to-goodness flagella. These organisms are found in ciliates (one in a Euplotes, another in a Paramecium ), where they display a peritrichous morphology. They carry out an active circular motion within their host's nucleoplasm in one case, and more or less linear motion in the cytoplasm in the other. Movement ceases when the host cells are crushed, so it may be confined to the interior of the cells. Why they move remains a mystery.
Chlamydiae and rickettsiae share flagellar genes but what else they have in common is not yet known. However, they share having a more sophisticated genetic complement than has been expected from 'simple' intracellular parasites. Motility may well be a common feature between them, albeit with distinctive characteristics in each kind. Are we surprised? Hardly. The microbial world tends to reveal increasing complexity and the more we study, the more surprising and often wondrous the things we uncover.
This paper was discussed in the October 12 episode (#162) of 'This Week in Microbiology' (TWiM). Press play to listen now.