Some thirty years ago it was my good fortune to sit in an airplane next to the famed marine microbiologist, the late Holger Jannasch, of the Woods Hole Oceanographic Institution. He shared with me stories of his deep-sea explorations, especially his voyages in the submersible Alvin. These included visits to the recently discovered deep sea hydrothermal vents and the amazing life forms that thrive in their vicinity.
The most spectacular of the denizens at these sites are the giant tube worms, Riftia pachyptila, which are white cylinders some 2 meters tall and ca. 4 cm thick. They are capped by red plumes (the name pachyptila comes from the Greek παχύς, "thick" and πτίλον, "feather"). A patch of Riftias may occupy tens of square meters, thus is visible from a distance to passengers in a vessel like Alvin.
Holger described the amazement caused when seeing arrays of these sizable structures after traveling for hours along the mostly barren sea floor. But before getting into this, let me recount his surprise at finding that when Alvin sank previously with no crewmen on board, their lunch of apples and baloney sandwiches was found upon recovery to be waterlogged but nearly intact. Holger understood that under those conditions of pressure and temperature, eubacteria metabolism was greatly slowed down.
Back to the giant tube worms. They sport a prominent top, a "branchial plume," its tentacles are red in color for being stuffed with hemoglobin (of all things), whereby oxygen and hydrogen sulfide are carried below, to the 'trophosome'. This is a vascularized tissue that pretty much fills the cavity. It contains billions of bacteria within specialized cells, the bacteriocytes. The bacteria are mutualistic symbionts that provide their host with the organic material they synthesize. A main source of nutrition for the worm are the bacteria themselves, which are eventually digested into usable compounds. The required energy is produced by the bacteria by oxidizing hydrogen sulfide, a form of autotrophic carbon fixation. It and oxygen are provided by the worm, which has no digestive system. In addition, the trophosome cells contain sulfur granules that likely serve as energy reserves.
R. pachyptila has a symbiotic relationship with a number of different autotrophic bacteria. One of the best studied is a gammaproteobacterium called Candidatus Endoriftia persephone (Candidatus means that it has not been cultivated yet). In sections of the trophosome, the bacteria are different in size: some are small rods, others large cocci. The smaller ones (ca. 2.0 to 5.0 microns in diameter) are found near the center of each lobule, close to a central blood vessel. The larger ones (5.0 to 20.0 microns) are located towards the periphery of the lobules, where they are eventually degraded and used for food. Only the small cells are able to divide, although the larger ones do replicate their DNA. The question arises, do these different kinds of cells of the same species carry out different metabolic functions? This is suggested by their high degree of metabolic redundancy, such as carrying the enzymes for two ways to fix carbon dioxide (the Calvin cycle and the reverse TCA cycle) and the enzymes for both making glycogen and degrading it. There is more, adding to the belief that these symbiotic bacteria may be heterogenous in their physiological functions and that they divide their tasks among them. Are these physiologies apportioned among the small and large bacteria? Isn't this hinted at by their distinct locations within the lobules of the trophosome?
In a recent paper (first author is Tjorven Hinzke, last author, Stephanie Markert), cells of the two cell types were isolated from trophosome tissue homogenates by gradient centrifugation and their proteomes analyzed. In addition, the bacteria were studied by fluorescence in situ hybridization, hybridization chain reaction, flow cytometry, and electron microscopy. The proteomic analysis told them that of some 2000 total symbiont proteins, 465 differed in abundance between the two cell types. These included proteins involved in the bacterial cell cycle and DNA replication and repair. FtsZ, DNA gyrase, and DNA binding proteins were more abundant in the small cells, while others that are involved in cell division (FtsE, MreB, SmlA) were increased in the large cells. Chaperones and the likes, outer membrane transport proteins, and proteins of carbon metabolism also showed differences in the two kinds of cells, as were proteins involved in chemotrophy. For the actual distribution of the proteins, see the article. Here you will also find a thorough discussion of the number of genome copies per cell (higher in the large symbionts) and chromosome compaction (lesser in the large cells). Also discussed are differences in symbionts rich in sulfur and depleted of it.
The authors also discuss the role of potential symbiosis-specific host proteins, the fact that the small symbionts may be exposed to higher stress levels and involved to a greater extent in host-microbe interactions. The division of labor goes something like this: Carbon fixation and biosynthesis are mainly the job of the large cells (in the words of one reviewer, they are the "workhorses," survival is the role of the small ones, the "stem cells"). The general conclusion is that the symbionts undergo different developmental stages, leading to physiological heterogeneity within their population.
Symbiotic bacteria do not stay put but frequently undergo differentiation. But rarely are they found in such a fascinating host as the giant tube worms, where they divide up their labors in such elegant manners. Giant tube worms are fascinating by themselves. The story of their symbionts adds considerably to their fascination.