Microfauna–Macrofauna Interaction in the Seafloor: Lessons from the Tubeworm

S ince their discovery in the 1970s and 1980s, giant tubeworms at hydrothermal vents and cold seeps have fascinated biologists and laymen alike—not only for their alien morphology (Figure 1), but also for epitomizing the perfect animal–microbe symbiosis. They are among the biggest worms on this planet—some over 3 m long— yet they do not eat other organisms. Tubeworms thrive independently of photosynthetic production [1]. They have even lost their entire digestive tract. One of the most exciting fi ndings in early tubeworm research was the discovery that the worm's food is delivered by bacterial symbionts [2]. The chemoautotrophic symbionts live intracellularly in a specialized worm tissue called the trophosome. They are sulfi de oxidizers, using the free energy yield from the oxidation of sulfi de with oxygen to fi x carbon dioxide with their bacterial Rubisco enzyme. In exchange for providing nutrition for the worm, the symbionts are sheltered from grazing, but most importantly, they receive a steady source of sulfi de and oxygen via the highly adapted blood circulation system of the worm. (I will never forget how horrifi ed I was as a young student by the amounts of almost human-like blood fl owing into my lab dish while dissecting tubeworms to analyze trophosome enzyme activity.) Tubeworm blood physiology, in particular the hemoglobin molecules, are tailored specifi cally to the needs of the symbionts. However, the host metabolism in itself is not different from that of many other animals, the main source of energy being aerobic respiration of carbohydrates. In other words, tubeworms and their symbionts need oxygen as an electron acceptor—so, after all, they are dependent on photosynthesis, the main oxygen-producing process on earth. With their strange morphology, vent tubeworms were fi rst classifi ed as a novel phylum, Vestimentifera [3]. Recently they have been regrouped together with the pogonophoran tubeworms (Figure 2) into a family of annelid polychaetes called the Siboglinidae [4,5]. Vestimentiferan tubeworms of hydrothermal vents grow on chimneys and other hard substrates in the vicinity of active vents, which emit reduced compounds like hydrogen and sulfi de [6]. Vestimentiferan tubeworms living at cold hydrocarbon seeps, i.e., the lamellibrachids and escarpids, are adapted to a sedimentary environment, with a substantial part of the body and tube of many species extending into the mud. All vestimentiferan tubeworms found today at vents, seeps, and a few other reduced submarine habitats harbor sulfi de-oxidizing endosymbionts in their …