Giant Tube Worm

''Riftia pachyptila'', commonly known as the giant tube worm and less commonly known as the Giant beardworm, is a marine invertebrate in the phylum Annelida (formerly grouped in phylum Pogonophora and Vestimentifera) related to tube worms commonly found in the intertidal and pelagic zones. ''R. pachyptila'' lives on the floor of the Pacific Ocean near hydrothermal vents, the vents provide a natural ambient temperature in their environment ranging from 2 to 30 °C, at the same time it can tolerate extremely high hydrogen sulfide levels. These worms can reach a length of , and their tubular bodies have a diameter of .

Its common name "giant tube worm" is, however, also applied to the largest living species of shipworm, ''Kuphus polythalamius'', which despite the name "worm", is a bivalve mollusc rather than an annelid.

Discovery

''R. pachyptila'' was discovered in 1977 on an expedition of the American bathyscaphe DSV ''Alvin'' to the Galápagos Rift led by geologist Jack Corliss. The discovery was unexpected, as the team was studying hydrothermal vents and no biologists were included in the expedition. Many of the species found living near hydrothermal vents during this expedition had never been seen before.

At the time, the presence of thermal springs near the midoceanic ridges was known. Further research uncovered aquatic life in the area, despite the high temperature (around 350–380 °C).

Many samples were collected, for example, bivalves, polychaetes, large crabs, and ''R. pachyptila''. It was the first time that species was observed.

Development

''R. pachyptila'' develops from a free-swimming, pelagic, nonsymbiotic trochophore larva, which enters juvenile (metatrochophore) development, becoming sessile, and subsequently acquiring symbiotic bacteria. The symbiotic bacteria, on which adult worms depend for sustenance, are not present in the gametes, but are acquired from the environment through the skin in a process akin to an infection. The digestive tract transiently connects from a mouth at the tip of the ventral medial process to a foregut, midgut, hindgut, and anus and was previously thought to have been the method by which the bacteria are introduced into adults. After symbionts are established in the midgut, they undergo substantial remodelling and enlargement to become the trophosome, while the remainder of the digestive tract has not been detected in adult specimens.

Body structure

Isolating the vermiform body from white chitinous tube, a small difference exists from the classic three subdivisions typical of phylum Pogonophora: the prosoma, the mesosoma, and the metasoma.

The first body region is the vascularized branchial plume, which is bright red due to the presence of hemoglobin that contain up to 144 globin chains (each presumably including associated heme structures). These tube worm hemoglobins are remarkable for carrying oxygen in the presence of sulfide, without being inhibited by this molecule, as hemoglobins in most other species are. The plume provides essential nutrients to bacteria living inside the trophosome. If the animal perceives a threat or is touched, it retracts the plume and the tube is closed due to the obturaculum, a particular operculum that protects and isolates the animal from the external environment.

The second body region is the vestimentum, formed by muscle bands, having a winged shape, and it presents the two genital openings at the end. The heart, extended portion of dorsal vessel, enclose the vestimentum.

In the middle part, the trunk or third body region, is full of vascularized solid tissue, and includes body wall, gonads, and the coelomic cavity. Here is located also the trophosome, spongy tissue where a billion symbiotic, thioautotrophic bacteria and sulfur granules are found. Since the mouth, digestive system, and anus are missing, the survival of ''R. pachyptila'' is dependent on this mutualistic symbiosis. This process, known as chemosynthesis, was recognized within the trophosome by Colleen Cavanaugh.

The soluble hemoglobins, present in the tentacles, are able to bind O₂ and H₂S, which are necessary for chemosynthetic bacteria. Due to the capillaries, these compounds are absorbed by bacteria. During the chemosynthesis, the mitochondrial enzyme rhodanase catalyzes the disproportionation reaction of the thiosulfate anion S₂O₃^2- to sulfur S and sulfite SO₃^2- . The ''R. pachyptila''’s bloodstream is responsible for absorption of the O₂ and nutrients such as carbohydrates.

Nitrate and nitrite are toxic, but are required for biosynthetic processes. The chemosynthetic bacteria within the trophosome convert nitrate to ammonium ions, which then are available for production of amino acids in the bacteria, which are in turn released to the tube worm. To transport nitrate to the bacteria, ''R. pachyptila'' concentrates nitrate in its blood, to a concentration 100 times more concentrated than the surrounding water. The exact mechanism of ''R. pachyptila''’s ability to withstand and concentrate nitrate is still unknown.

In the posterior part, the fourth body region, is the opistosome, which anchors the animal to the tube and is used for the storage of waste from bacterial reactions.

Symbiosis

The discovery of bacterial invertebrate chemoautotrophic symbiosis, particularly in vestimentiferan tubeworms ''R. pachyptila'' and then in vesicomyid clams and mytilid mussels revealed the chemoautotrophic potential of the hydrothermal vent tube worm. Scientists discovered a remarkable source of nutrition that helps to sustain the conspicuous biomass of invertebrates at vents. Many studies focusing on this type of symbiosis revealed the presence of chemoautotrophic, endosymbiotic, sulfur-oxidizing bacteria mainly in ''R. pachyptila'', which inhabits extreme environments and is adapted to the particular composition of the mixed volcanic and sea waters. This special environment is filled with inorganic metabolites, essentially carbon, nitrogen, oxygen, and sulfur. In its adult phase, ''R. pachyptila'' lacks a digestive system. To provide its energetic needs, it retains those dissolved inorganic nutrients (sulfide, carbon dioxide, oxygen, nitrogen) into its plume and transports them through a vascular system to the trophosome, which is suspended in paired coelomic cavities and is where the intracellular symbiotic bacteria are found. The trophosome is a soft tissue that runs through almost the whole length of the tube's coelom. It retains a large number of bacteria on the order of 10⁹ bacteria per gram of fresh weight. Bacteria in the trophosome are retained inside bacteriocytes, thereby having no contact with the external environment. Thus, they rely on ''R. pachyptila'' for the assimilation of nutrients needed for the array of metabolic reactions they employ and for the excretion of waste products of carbon fixation pathways. At the same time, the tube worm depends completely on the microorganisms for the byproducts of their carbon fixation cycles that are needed for its growth.

Initial evidence for a chemoautotrophic symbiosis in ''R. pachyptila'' came from microscopic and biochemical analyses showing Gram-negative bacteria packed within a highly vascularized organ in the tubeworm trunk called the trophosome. Additional analyses involving stable isotope, enzymatic, and physiological characterizations confirmed that the end symbionts of ''R. pachyptila'' oxidize reduced-sulfur compounds to synthesize ATP for use in autotrophic carbon fixation through the Calvin cycle. The host tubeworm enables the uptake and transport of the substrates required for thioautotrophy, which are HS⁻, O₂, and CO₂, receiving back a portion of the organic matter synthesized by the symbiont population. The adult tubeworm, given its inability to feed on particulate matter and its entire dependency on its symbionts for nutrition, the bacterial population is then the primary source of carbon acquisition for the symbiosis. Discovery of bacterial–invertebrate chemoautotrophic symbioses, initially in vestimentiferan tubeworms and then in vesicomyid clams and mytilid mussels, pointed to an even more remarkable source of nutrition sustaining the invertebrates at vents.

Endosymbiosis with chemoautotrophic bacteria

A wide range of bacterial diversity is associated with symbiotic relationships with ''R. pachyptila''. Many bacteria belong to the phylum Campylobacterota (formerly class Epsilonproteobacteria) as supported by the recent discovery in 2016 of the new species ''Sulfurovum riftiae'' belonging to the phylum Campylobacterota, family Helicobacteraceae isolated from ''R. pachyptila'' collected from the East Pacific Rise. Other symbionts belong to the class Delta-, Alpha- and Gammaproteobacteria. The ''Candidatus'' Endoriftia persephone (Gammaproteobacteria) is a facultative ''R. pachyptila'' symbiont and has been shown to be a mixotroph, thereby exploiting both Calvin Benson cycle and reverse TCA cycle (with an unusual ATP citrate lyase) according to availability of carbon resources and whether it is free living in the environment or inside a eukaryotic host. The bacteria apparently prefer a heterotrophic lifestyle when carbon sources are available.

Evidence based on 16S rRNA analysis affirms that ''R. pachyptila'' chemoautotrophic bacteria belong to two different clades: Gammaproteobacteria and Campylobacterota (e.g. ''Sulfurovum riftiae'') that get energy from the oxidation of inorganic sulfur compounds such as hydrogen sulfide (H₂S, HS⁻, S^2-) to synthetize ATP for carbon fixation via the Calvin cycle. Unfortunately, most of these bacteria are still uncultivable. Symbiosis works so that ''R. pachyptila'' provides nutrients such as HS⁻, O₂, CO₂ to bacteria, and in turn it receives organic matter from them. Thus, because of lack of a digestive system, ''R. pachyptila'' depends entirely on its bacterial symbiont to survive.

In the first step of sulfide-oxidation, reduced sulfur (HS⁻) passes from the external environment into ''R. pachyptila'' blood, where, together with O₂, it is bound by hemoglobin, forming the complex Hb-O₂-HS⁻ and then it is transported to the trophosome, where bacterial symbionts reside. Here, HS⁻ is oxidized to elemental sulfur (S⁰) or to sulfite (SO₃^2-).

In the second step, the symbionts make sulfite-oxidation by the "APS pathway", to get ATP. In this biochemical pathway, AMP reacts with sulfite in the presence of the enzyme APS reductase, giving APS (adenosine 5'-phosphosulfate). Then, APS reacts with the enzyme ATP sulfurylase in presence of pyrophosphate (PPi) giving ATP ( substrate-level phosphorylation) and sulfate (SO₄^2-) as end products. In formulas:

* AMP + SO3^2- -> PSreductaseAPS
* APS + PPi -> TP sulfurylaseATP + SO4^2-

The electrons released during the entire sulfide-oxidation process enter in an electron transport chain, yielding a proton gradient that produces ATP ( oxydative phosphorylation). Thus, ATP generated from oxidative phosphorylation and ATP produced by substrate-level phosphorylation become available for CO₂ fixation in Calvin cycle, whose presence has been demonstrated by the presence of two key enzymes of this pathway: phosphoribulokinase and RubisCO.

To support this unusual metabolism, ''R. pachyptila'' has to absorb all the substances necessary for both sulfide-oxidation and carbon fixation, that is: HS⁻, O₂ and CO₂ and other fundamental bacterial nutrients such as N and P. This means that the tubeworm must be able to access both oxic and anoxic areas.

Oxidation of reduced sulfur compounds requires the presence of oxidized reagents such as oxygen and nitrate. Hydrothermal vents are characterized by conditions of high hypoxia. In hypoxic conditions, sulfur-storing organisms start producing hydrogen sulfide. Therefore, the production of in H₂S in anaerobic conditions is common among thiotrophic symbiosis. H₂S can be damaging for some physiological processes as it inhibits the activity of cytochrome c oxidase, consequentially impairing oxidative phosphorilation. In ''R. pachyptila'' the production of hydrogen sulfide starts after 24h of hypoxia. In order to avoid physiological damage some animals, including ''Riftia'' ''pachyptila'' are able to bind H₂S to haemoglobin in the blood to eventually expel it in the surrounding environment.

Carbon fixation and organic carbon assimilation

Unlike metazoans, which respire carbon dioxide as a waste product, ''R. pachyptila''-symbiont association has a demand for a net uptake of CO₂ instead, as a cnidarian-symbiont associations.

Ambient deep-sea water contains an abundant amount of inorganic carbon in the form of bicarbonate HCO₃⁻, but it is actually the chargeless form of inorganic carbon, CO₂, that is easily diffusible across membranes. The low partial pressures of CO₂ in the deep-sea environment is due to the seawater alkaline pH and the high solubility of CO₂, yet the pCO₂ of the blood of ''R. pachyptila'' may be as much as two orders of magnitude greater than the pCO₂ of deep-sea water.

CO₂ partial pressures are transferred to the vicinity of vent fluids due to the enriched inorganic carbon content of vent fluids and their lower pH. CO₂ uptake in the worm is enhanced by the higher pH of its blood (7.3–7.4), which favors the bicarbonate ion and thus promotes a steep gradient across which CO₂ diffuses into the vascular blood of the plume. The facilitation of CO₂ uptake by high environmental pCO₂ was first inferred based on measures of elevated blood and coelomic fluid pCO₂ in tubeworms, and was subsequently demonstrated through incubations of intact animals under various pCO₂ conditions.

Once CO₂ is fixed by the symbionts, it must be assimilated by the host tissues. The supply of fixed carbon to the host is transported via organic molecules from the trophosome in the hemolymph, but the relative importance of translocation and symbiont digestion is not yet known. Studies proved that within 15 min, the label first appears in symbiont-free host tissues, and that indicates a significant amount of release of organic carbon immediately after fixation. After 24 h, labeled carbon is clearly evident in the epidermal tissues of the body wall. Results of the pulse-chase autoradiographic experiments were also evident with ultrastructural evidence for digestion of symbionts in the peripheral regions of the trophosome lobules.

Sulfide acquisition

In deep-sea hydrothermal vents, sulfide and oxygen are present in different areas. Indeed, the reducing fluid of hydrothermal vents is rich in sulfide, but poor in oxygen, whereas sea water is richer in dissolved oxygen. Moreover, sulfide is immediately oxidized by dissolved oxygen to form partly, or totally, oxidized sulfur compounds like thiosulfate (S₂O₃^2-) and ultimately sulfate (SO₄^2-), respectively less, or no longer, usable for microbial oxidation metabolism. This causes the substrates to be less available for microbial activity, thus bacteria are constricted to compete with oxygen to get their nutrients. In order to avoid this issue, several microbes have evolved to make symbiosis with eukaryotic hosts. In fact, ''R. pachyptila'' is able to cover the oxic

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