Concept: Hydrothermal vent
Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 2 years ago
The “wooden-steps” hypothesis [Distel DL, et al. (2000) Nature 403:725-726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalve Kuphus polythalamia This rare and enigmatic species, which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show that K. polythalamia harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate that K. polythalamia is a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example in which a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.
Hydrothermal vents in the Southern Ocean are the physiologically most isolated chemosynthetic environments known. Here, we describe Kiwa tyleri sp. nov., the first species of yeti crab known from the Southern Ocean. Kiwa tyleri belongs to the family Kiwaidae and is the visually dominant macrofauna of two known vent sites situated on the northern and southern segments of the East Scotia Ridge (ESR). The species is known to depend on primary productivity by chemosynthetic bacteria and resides at the warm-eurythermal vent environment for most of its life; its short-range distribution away from vents (few metres) is physiologically constrained by the stable, cold waters of the surrounding Southern Ocean. Kiwa tylerihas been shown to present differential life history adaptations in response to this contrasting thermal environment. Morphological adaptations specific to life in warm-eurythermal waters, as found on - or in close proximity of - vent chimneys, are discussed in comparison with adaptations seen in the other two known members of the family (K. hirsuta, K. puravida), which show a preference for low temperature chemosynthetic environments.
The Mid-Cayman spreading centre is an ultraslow-spreading ridge in the Caribbean Sea. Its extreme depth and geographic isolation from other mid-ocean ridges offer insights into the effects of pressure on hydrothermal venting, and the biogeography of vent fauna. Here we report the discovery of two hydrothermal vent fields on the Mid-Cayman spreading centre. The Von Damm Vent Field is located on the upper slopes of an oceanic core complex at a depth of 2,300 m. High-temperature venting in this off-axis setting suggests that the global incidence of vent fields may be underestimated. At a depth of 4,960 m on the Mid-Cayman spreading centre axis, the Beebe Vent Field emits copper-enriched fluids and a buoyant plume that rises 1,100 m, consistent with >400 °C venting from the world’s deepest known hydrothermal system. At both sites, a new morphospecies of alvinocaridid shrimp dominates faunal assemblages, which exhibit similarities to those of Mid-Atlantic vents.
Although it is not known when or where life on Earth began, some of the earliest habitable environments may have been submarine-hydrothermal vents. Here we describe putative fossilized microorganisms that are at least 3,770 million and possibly 4,280 million years old in ferruginous sedimentary rocks, interpreted as seafloor-hydrothermal vent-related precipitates, from the Nuvvuagittuq belt in Quebec, Canada. These structures occur as micrometre-scale haematite tubes and filaments with morphologies and mineral assemblages similar to those of filamentous microorganisms from modern hydrothermal vent precipitates and analogous microfossils in younger rocks. The Nuvvuagittuq rocks contain isotopically light carbon in carbonate and carbonaceous material, which occurs as graphitic inclusions in diagenetic carbonate rosettes, apatite blades intergrown among carbonate rosettes and magnetite-haematite granules, and is associated with carbonate in direct contact with the putative microfossils. Collectively, these observations are consistent with an oxidized biomass and provide evidence for biological activity in submarine-hydrothermal environments more than 3,770 million years ago.
Deep-sea hydrothermal vents are subject to major disturbances that alter the physical and chemical environment and eradicate the resident faunal communities. Vent fields are isolated by uninhabitable deep seafloor, so recolonization via dispersal of planktonic larvae is critical for persistence of populations. We monitored colonization near 9°50'N on the East Pacific Rise following a catastrophic eruption in order to address questions of the relative contributions of pioneer colonists and environmental change to variation in species composition, and the role of pioneers at the disturbed site in altering community structure elsewhere in the region. Pioneer colonists included two gastropod species: Ctenopelta porifera, which was new to the vent field, and Lepetodrilus tevnianus, which had been rare before the eruption but persisted in high abundance afterward, delaying and possibly out-competing the ubiquitous pre-eruption congener L. elevatus. A decrease in abundance of C. porifera over time, and the arrival of later species, corresponded to a decrease in vent fluid flow and in the sulfide to temperature ratio. For some species these successional changes were likely due to habitat requirements, but other species persisted (L. tevnianus) or arrived (L. elevatus) in patterns unrelated to their habitat preferences. After two years, disturbed communities had started to resemble pre-eruption ones, but were lower in diversity. When compared to a prior (1991) eruption, the succession of foundation species (tubeworms and mussels) appeared to be delayed, even though habitat chemistry became similar to the pre-eruption state more quickly. Surprisingly, a nearby community that had not been disturbed by the eruption was invaded by the pioneers, possibly after they became established in the disturbed vents. These results indicate that the post-eruption arrival of species from remote locales had a strong and persistent effect on communities at both disturbed and undisturbed vents.
BACKGROUND: The inhabitants of deep-sea hydrothermal vents occupy ephemeral island-like habitats distributed sporadically along tectonic spreading-centers, back-arc basins, and volcanically active seamounts. The majority of vent taxa undergo a pelagic larval phase, and thus varying degrees of geographical subdivision, ranging from no impedance of dispersal to complete isolation, often exist among taxa that span common geomorphological boundaries. Two lineages of Bathymodiolus mussels segregate on either side of the Easter Microplate, a boundary that separates the East Pacific Rise from spreading centers connected to the Pacific-Antarctic Ridge. RESULTS: A recent sample from the northwest flank of the Easter Microplate contained an admixture of northern and southern mitochondrial haplotypes and corresponding alleles at five nuclear gene loci. Genotypic frequencies in this sample did not fit random mating expectation. Significant heterozygote deficiencies at nuclear loci and gametic disequilibria between loci suggested that this transitional region might be a ‘Tension Zone’ maintained by immigration of parental types and possibly hybrid unfitness. An analysis of recombination history in the nuclear genes suggests a prolonged history of parapatric contact between the two mussel lineages. We hereby elevate the southern lineage to species status as Bathymodiolus antarcticus n. sp. and restrict the use of Bathymodiolus thermophilus to the northern lineage. CONCLUSIONS: Because B. thermophilus s.s. exhibits no evidence for subdivision or isolation-by-distance across its 4000 km range along the EPR axis and Galapagos Rift, partial isolation of B. antarcticus n. sp. requires explanation. The time needed to produce the observed degree of mitochondrial differentiation is consistent with the age of the Easter Microplate (2.5 to 5.3 million years). The complex geomorphology of the Easter Microplate region forces strong cross-axis currents that might disrupt self-recruitment of mussels by removing planktotrophic larvae from the ridge axis. Furthermore, frequent local extinction events in this tectonically dynamic region might produce a demographic sink rather than a source for dispersing mussel larvae. Historical changes in tectonic rates and current patterns appear to permit intermittent contact and introgression between the two subspecies.
The Southwest Indian Ridge is the longest section of very slow to ultraslow-spreading seafloor in the global mid-ocean ridge system, but the biogeography and ecology of its hydrothermal vent fauna are previously unknown. We collected 21 macro- and megafaunal taxa during the first Remotely Operated Vehicle dives to the Longqi vent field at 37° 47’S 49° 39'E, depth 2800 m. Six species are not yet known from other vents, while six other species are known from the Central Indian Ridge, and morphological and molecular analyses show that two further polychaete species are shared with vents beyond the Indian Ocean. Multivariate analysis of vent fauna across three oceans places Longqi in an Indian Ocean province of vent biogeography. Faunal zonation with increasing distance from vents is dominated by the gastropods Chrysomallon squamiferum and Gigantopelta aegis, mussel Bathymodiolus marisindicus, and Neolepas sp. stalked barnacle. Other taxa occur at lower abundance, in some cases contrasting with abundances at other vent fields, and δ(13)C and δ(15)N isotope values of species analysed from Longqi are similar to those of shared or related species elsewhere. This study provides baseline ecological observations prior to mineral exploration activities licensed at Longqi by the United Nations.
The discovery of deep-sea hydrothermal vents in 1977 challenged our views of ecosystem functioning and yet, the research conducted at these extreme and logistically challenging environments still continues to reveal unique biological processes. Here, we report for the first time, a unique behavior where the deep-sea skate, Bathyraja spinosissima, appears to be actively using the elevated temperature of a hydrothermal vent environment to naturally “incubate” developing egg-cases. We hypothesize that this behavior is directly targeted to accelerate embryo development time given that deep-sea skates have some of the longest egg incubation times reported for the animal kingdom. Similar egg incubating behavior, where eggs are incubated in volcanically heated nesting grounds, have been recorded in Cretaceous sauropod dinosaurs and the rare avian megapode. To our knowledge, this is the first time incubating behavior using a volcanic source is recorded for the marine environment.
The ca. 3.48 Ga Dresser Formation, Pilbara Craton, Western Australia, is well known for hosting some of Earth’s earliest convincing evidence of life (stromatolites, fractionated sulfur/carbon isotopes, microfossils) within a dynamic, low-eruptive volcanic caldera affected by voluminous hydrothermal fluid circulation. However, missing from the caldera model were surface manifestations of the volcanic-hydrothermal system (hot springs, geysers) and their unequivocal link with life. Here we present new discoveries of hot spring deposits including geyserite, sinter terracettes and mineralized remnants of hot spring pools/vents, all of which preserve a suite of microbial biosignatures indicative of the earliest life on land. These include stromatolites, newly observed microbial palisade fabric and gas bubbles preserved in inferred mineralized, exopolymeric substance. These findings extend the known geological record of inhabited terrestrial hot springs on Earth by ∼3 billion years and offer an analogue in the search for potential fossil life in ancient Martian hot springs.
Since the first discovery of deep-sea hydrothermal vents along the Galápagos Rift in 1977, numerous vent sites and endemic faunal assemblages have been found along mid-ocean ridges and back-arc basins at low to mid latitudes. These discoveries have suggested the existence of separate biogeographic provinces in the Atlantic and the North West Pacific, the existence of a province including the South West Pacific and Indian Ocean, and a separation of the North East Pacific, North East Pacific Rise, and South East Pacific Rise. The Southern Ocean is known to be a region of high deep-sea species diversity and centre of origin for the global deep-sea fauna. It has also been proposed as a gateway connecting hydrothermal vents in different oceans but is little explored because of extreme conditions. Since 2009 we have explored two segments of the East Scotia Ridge (ESR) in the Southern Ocean using a remotely operated vehicle. In each segment we located deep-sea hydrothermal vents hosting high-temperature black smokers up to 382.8°C and diffuse venting. The chemosynthetic ecosystems hosted by these vents are dominated by a new yeti crab (Kiwa n. sp.), stalked barnacles, limpets, peltospiroid gastropods, anemones, and a predatory sea star. Taxa abundant in vent ecosystems in other oceans, including polychaete worms (Siboglinidae), bathymodiolid mussels, and alvinocaridid shrimps, are absent from the ESR vents. These groups, except the Siboglinidae, possess planktotrophic larvae, rare in Antarctic marine invertebrates, suggesting that the environmental conditions of the Southern Ocean may act as a dispersal filter for vent taxa. Evidence from the distinctive fauna, the unique community structure, and multivariate analyses suggest that the Antarctic vent ecosystems represent a new vent biogeographic province. However, multivariate analyses of species present at the ESR and at other deep-sea hydrothermal vents globally indicate that vent biogeography is more complex than previously recognised.