Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms

Abstract

Deep-sea vestimentiferan tubeworms, which live in symbiosis with bacteria, exhibit different life strategies according to their habitat. At unstable and relatively short-lived hydrothermal vents, they grow extremely fast, whereas their close relatives at stable and long-persisting cold seeps grow slowly and live up to 300 years. Growth and age differences are thought to occur because of ecological and physiological adaptations. However, the underlying mechanisms of cell proliferation and death, which are closely linked to homeostasis, growth, and longevity, are unknown. Here, we show by immunohistochemical and ultrastructural cell cycle analyses that cell proliferation activities of the two species studied are higher than in any other characterized invertebrate, being only comparable with tumor and wound-healing processes. The slow growth in Lamellibrachia luymesi from cold seeps results from balanced activities of proliferation and apoptosis in the epidermis. In contrast, Riftia pachyptila from hydrothermal vents grows fast because apoptosis is down-regulated in this tissue. The symbiont-housing organ, the trophosome, exhibits a complex cell cycle and terminal differentiation pattern in both species, and growth is regulated by proliferation. These mechanisms have similarities to the up- and down-regulation of proliferation or apoptosis in various types of tumor, although they occur in healthy animals in this study, thus providing significant insights into the underlying mechanisms of growth and longevity.

Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population

“…In contrast to restricted proliferation of rods and small cocci in the trophosome (43), all morphotypes of the released symbionts apparently divided after release and settling on surfaces (Fig. 2B), and the majority of proliferating symbionts were large cocci.…”

“…Additionally, filtered water sampled before the experiments was checked by FISH and 16S rRNA gene PCR (SI Materials and Methods) using the symbiontspecific probe RifTO445 and the primers RifTO44 and RifTO445, respectively (30,34). For TEM investigations, 30 randomly selected pictures were taken from the central and median lobule zones (43) of each trophosome with a Zeiss EM 902 transmission electron microscope. The average of symbiont counts for each replicate and each treatment, as well as the percentages compared with the freshly fixed trophosome under initial conditions taken as 100%, is listed in Table S2 (Fig.…”

“…The observed connectivity of host-associated and free-living symbiont populations helps to explain the stability of this mutualism over ecological and evolutionary timescales. (25-27) partnerships, in Riftia there is no support for such a release (44), and it has been suggested that the vast majority of symbionts are terminally differentiated during the host's life (43).…”

“…The intracellular symbionts are located in specialized host cells, the bacteriocytes, deep within the host body with no openings toward the exterior (40)(41)(42). The bacteria divide within unipotent bacteriocyte stem cells mostly as rods, convert into small and large cocci in the proliferating bacteriocytes, and are digested before host bacteriocyte apoptosis (43). Whereas in some mutualisms, release of symbionts may happen during the host's life, such as in the V. fischeri-squid (23,24) and rhizobia-legume…”

Evolutionary transitions in bacterial symbiosis

“…Second, bacterial mutualists inhabit diverse host tissues ranging from skin, mucosa, leaves, and roots to inter-and intracellular spaces. Some bacterial mutualists inhabit specialized structures in hosts (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26), whereas others range widely in host mucosa or other unstructured tissues (27)(28)(29) (Table 1). Finally, bacterial mutualists provide a great variety of benefits to hosts, including nutrients (15,17,20,26,27,30), bioluminescence (14), and antibiotic production (31)(32)(33).…”