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

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. Financial support was provided by the Austrian Science Foundation (FWF; grants to M.B.), a DOC scholarship from the Austrian Academy of Science (to B.P.), and grants from the US National Science Foundation (to C.R. Fisher).     

Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents

Population genetic and phylogenetic analyses of mitochondrial COI from five deep-sea hydrothermal vent annelids provided insights into their dispersal modes and barriers to gene flow. These polychaetes inhabit vent fields located along the East Pacific Rise (EPR) and Galapagos Rift (GAR), where hundreds to thousands of kilometers can separate island-like populations. Long-distance dispersal occurs via larval stages, but larval life histories differ among these taxa. Mitochondrial gene flow between populations of Riftia pachyptila, a siboglinid worm with neutrally buoyant lecithothrophic larvae, is diminished across the Easter Microplate region, which lies at the boundary of Indo-Pacific and Antarctic deep-sea provinces. Populations of the siboglinid Tevnia jerichonana are similarly subdivided. Oasisia alvinae is not found on the southern EPR, but northern EPR populations of this siboglinid are subdivided across the Rivera Fracture Zone. Mitochondrial gene flow of Alvinella pompejana, an alvinellid with large negatively buoyant lecithotrophic eggs and arrested embryonic development, is unimpeded across the Easter Microplate region. Gene flow in the polynoid Branchipolynoe symmytilida also is unimpeded across the Easter Microplate region. However, A. pompejana populations are subdivided across the equator, whereas B. symmitilida populations are subdivided between the EPR and GAR axes. The present findings are compared with similar evidence from codistributed species of annelids, molluscs and crustaceans to identify potential dispersal filters in these eastern Pacific ridge systems.     

Ribulose bisphosphate carboxylase of the procaryotic symbiont of a hydrothermal vent tube worm: kinetics, activity and gene hybridization

Abstract The giant tube worm, Riftia pachyptila , which is abundant at deep-sea hydrothermal vents, contains an extremely high density of bacterial symbionts in a specialized 'trophosome' tissue. Although the symbiont has not been cultured, enzymatic studies by others indicate that the symbiont is capable of hydrogen-sulfide- or sulfur-based lithoautotrophy and fixes CO₂ via the Calvin-Benson cycle. Here we report additional findings for a specimen from the Guaymas Basin vent site (Gulf of California, 2000 m). Under assay conditions where activity was proportional to cell-free extract concentration, ribulose bisphosphate carboxylase/oxygenase (RuBisCO) activity was 6.3 nmol CO₂/mg protein per min (30°C). This is within the range observed for non-CO₂ limited cultures of sulfur bacteria. The activity vs. temperature profile suggests that the symbiont is a mesophile and not a thermophile. A substrate saturation curve shows an apparent K _m (with respect to ribulose 1,5-bisphosphate) of 65 μM which is considerably lower than the single previous report for a sulfur bacterial symbiont. Strong hybridization was detected between a gene probe derived from the RuBisCO large subunit gene of Anacystis nidulans and Riftia trophosome DNA. A Rhodospirillum rubrum -derived probe also showed hybridization with the same restriction fragments of symbiont DNA.     

Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error?

Species colonizing new deep-sea hydrothermal vents along the East Pacific Rise show a distinct successional sequence: pioneer assemblages dominated by the vestimentiferan tubeworm Tevnia jerichonana being subsequently invaded by another vestimentiferan Riftia pachyptila, and eventually the mussel Bathymodiolus thermophilus. Using a manipulative approach modified from shallow-water ecological studies, we test three alternative hypotheses to explain the initial colonization by T. jerichonana and its subsequent replacement by R. pachyptila. We show that R. pachyptila and another vestimentiferan, Oasisia alvinae, colonized new surfaces only if the surfaces also were colonized by T. jerichonana. This pattern does not appear to be due to restricted habitat tolerances or inferior dispersal capabilities of R. pachyptila and O. alvinae, and we argue the alternative explanation that T. jerichonana facilitates the settlement of the other two species and is eventually outcompeted by R. pachyptila. Unlike the classic model of community succession, in which facilitating species promote their own demise by modifying the environment to make it more hospitable for competitors, we suggest that T. jerichonana may produce a chemical substance that induces settlement of these competitors. This process of selecting habitat based on biogenic cues may be especially adaptive and widespread among later-successional species that occupy a physically variable and unpredictable environment. In these cases, the presence of weedy species implies some integrated period of environmental suitability, whereas an instantaneous assessment of physical habitat conditions, such as water temperature for vent tubeworms, provides a poorer predictor of long-term habitat suitability. Received: 13 July 1999 / Accepted: 2 November 1999     

Thermococcus chitonophagus sp. nov., a novel,chitin-degrading,hyperthermophilic archaeum from a deep-sea hydrothermal vent environment

From a hydrothermal vent site off the Mexican west coast (20°50′N, 109°06′W) at a depth of 2,600 m, a novel, hyperthermophilic, anaerobic archaeum was isolated. Cells were round to slightly irregular cocci, 1.2–2.5 μm in diameter and were motile by means of a tuft of flagella. The new isolate grew between 60 and 93°C (optimum: 85°C), from pH 3.5 to 9 (optimum: pH 6.7), and from 0.8 to 8% NaCl (optimum: 2%). The isolate was an obligate organotroph, using chitin, yeast extract, meat extract, and peptone for growth. Chitin was fermented to H₂, CO₂, NH₃, acetate, and formate. H₂S was formed in the presence of sulfur. The chitinoclastic enzyme system was oxygen-stable, cell-associated, and inducible by chitin. The cell wall was composed of a surface layer of hex- americ protein complexes arranged on a p6 lattice. The core lipids consisted of glycerol diphytanyl diethers and acyclic and cyclic glycerol diphytanyl tetraethers. The G+C content was 46.5 mol%. DNA/DNA hybridization and 16S rRNA sequencing indicated that the new isolate belongs to the genus Thermococcus, representing a new species, Thermococcus chitonophagus. The type strain is isolate GC74, DSM 10152. Received: 8 May 1995 / Accepted: 26 June 1995     

Epidermal ultrastructure and implications for sulfide tolerance in six species of deep-sea polychaetes

Abstract. Ultrastructural characteristics of the epidermis of 5 deep-sea vestimentiferan tube worms and an orbiniid worm were similar to those described from other organisms inhabiting sulfidic environments. The integument was composed of a simple or pseudostratified layer of columnar or cuboidal cells, covered by a cuticle of varying thickness, and rested on an extracellular matrix. Unusual mitochondrial morphology was observed in the peripheral region of the epidermis, characterized by an electron-dense matrix and granules. The abnormal size, shape, and reduced array of cristae in these mitochondria may have resulted from environmental stress. Mitochondria in the inner epidermal layers, where they are more protected from sulfide exposure, displayed normal morphology. The seep vestimentiferans ( Seepiophila jonesi and Lamellibrachia cf. luymesi ) exhibited numerous electron-dense organelles, similar in morphology to cytolysosomes and previously described as sulfide oxidizing bodies, while in the 3 vent vestimentiferans ( Riftia pachyptila, Tevnia jerichonana , and Oasisia alvinae ) and the seep orbiniid Methanoaricia dendrobranchiata , fewer of these organelles were observed. Energy dispersive x-ray microanalysis of these electron-dense organelles indicated the presence of sulfur, iron, zinc, and copper, as well as lesser amounts of other elements. We propose that these epidermal cytolysosomes are morphologically similar to previously described sulfide oxidizing bodies that have been hypothesized to play a role in maintaining aerobically poised animal metabolism in sulfide-enriched habitats.     

Development and characterization of 12 microsatellite markers from the deep-sea hydrothermal vent siboglinid Riftia pachyptila

Ecological processes at deep‐sea hydrothermal vents on fast‐spreading mid‐ocean ridges are punctuated by frequent physical disturbance, often accompanied by a high occurrence of population turnover. To persist through local extinction events, sessile invertebrate species living in these geologically and chemically dynamic habitats depend on larval dispersal. We characterized 12 polymorphic microsatellite loci from one such species, the siboglinid tubeworm Riftia pachyptila. All loci conformed to Hardy–Weinberg expectations without linkage (mean H_E = 0.9405, mean N_A = 20.25). These microsatellites are being employed in the investigation of spatial and temporal population genetic structure in the eastern Pacific Ocean.