Riftia pachyptila

Riftia pachyptila, commonly known as giant tube worms, are marine invertebrates in the phylum Annelida[1] (formerly `grouped in phylum Pogonophora and Vestimentifera) related to tube worms commonly found in the intertidal and pelagic zones. Riftia pachyptila live on the floor of the Pacific Ocean near hydrothermal vents, and can tolerate extremely high hydrogen sulfide levels. These worms can reach a length of 3 m (9 ft 10 in),[2] and their tubular bodies have a diameter of 4 cm (1.6 in). Ambient temperature in their natural environment ranges from 2 to 30 degrees Celsius.[3]

Giant tube worms
Scientific classification
Kingdom:
Animalia
Phylum:
Annelida
Class:
Polychaeta
Order:
Canalipalpata
Family:
Siboglinidae
Genus:
Riftia
Species:
R. pachyptila
Binomial name
Riftia pachyptila
M. L. Jones, 1981

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

DSV ALVIN, the Navy research submarine

Discovery

Riftia pachyptila were discovered in 1977 on an expedition of the American bathyscaphe DSV Alvin to the Galápagos Rift led by geologist Jack Corliss.[4] The discovery was unexpected, as the team were 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 mid oceanic ridges was known. Further research uncovered aquatic life in the area, despite the high temperature (around 350 °C – 380 °C).[5][6]

Many samples were collected, for example, bivalves, polychaetes, large crabs and Riftia pachyptila.[7][8] It was the first time that Riftia pachyptila was observed.

Development

Riftia develop from a free-swimming, pelagic, non-symbiotic trochophore larva, which enters juvenile (metatrochophore) development, becoming sessile and subsequently acquiring symbiotic bacteria.[9][10] The symbiotic bacteria, on which adult worms depend for sustenance, are not present in the gametes, but are acquired from the environment via 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 is introduced into adults. After symbionts are established in the midgut, it undergoes substantial remodelling and enlargement to become the trophosome, while the remainder of the digestive tract has not been detected in adult specimens.[11]

Body structure
Hydrothermal vent tubeworms get organic compounds from bacteria that live in their trophosome.

Isolating the vermiform body from white chitonous tube, there is a small difference from the classic three subdivisions typical of phylum Pogonophora:[12] the prosoma, the mesosoma, and the metasoma.

Riftia pachyptila community with extroflexion of red branchial plume.

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.[13][14] 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 thanks to the obturaculum, a particular operculum which protects and isolates the animal from the external environment.[15]

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.[16][17] The heart, extended portion of dorsal vessel, enclose the vestimentum.[18]

In the middle part there is the trunk, third body region, full of vascularized solid tissue and which includes body wall, gonads, and the coelomic cavity. Here is located also the trophosome, spongy tissue where there is a billion of symbiotic Thioautotrophic Bacteria and sulfur granules.[19][20] Since the mouth, digestive system and anus are missing, the survival of R. pachyptila is guaranteed by this mutualistic symbiosis.[21] This process, known as chemosynthesis, was recognized within the trophosome by Colleen Cavanaugh.[21]

The soluble hemoglobins, present in the tentacles, are able to bind O2 and H2S, which are necessary for chemosynthetic bacteria. Thanks to the capillaries these compounds are absorbed by bacteria.[22] During the chemosynthesis, the mitochondrial enzyme rhodanase catalyzes the disproportionation reaction of the thiosulfate anion S2O32- to sulfur S and sulfite SO32- .[23][24] The R. pachyptila’s bloodstream is responsible for absorption the products like O2 and nutrients like carbohydrates.

Nitrate and nitrite are toxic, but nitrogen is required for biosynthetic processes. The chemosynthetic bacteria within the trophosome convert this 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 concentrate nitrate in their 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.[14]

In the posterior part, the fourth body region, there is opistosome, which anchor the animal to the tube and it is used for the storage of waste from bacterial reactions.[25]

Symbiosis

The discovery of bacterial invertebrate chemoautotrophic symbiosis, particularly in vestimentiferan tubeworms Riftia pachyptila[21] and then in vesicomyidae clams and mytilid mussels revealed the chemoautotrophic potential of the hydrothermal vent tube worm.[26] Scientists discovered a remarkable source of nutrition, that helps to maintain the sustainability of the conspicuous biomass of invertebrates at vents.[26] Many studies focusing on this type of symbiosis revealed the presence of chemoautotrophic, endosymbiotic, sulfur-oxidizing bacteria mainly in Riftia pachyptila,[27] which inhabitates extreme environments and is adapted to the particular composition of the mixed volcanic and sea waters.[28] This special environment is fullfilled with inorganic metabolites, essentially carbon, nitrogen, oxygen and sulfur. In its adult phase, Riftia pachyptila lack a digestive system. In order to provide its energetic needs, it retains those dissolved inorganic nutrients (sulfide, carbon dioxide, oxygen, nitrogen) into 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.[20][29][30] The trophosome[31] is a soft tissue that runs through almost the whole length of the tube's coelom. It retains a large number of bacteria in the order of 109 bacteria per gram of fresh weight.[32] Bacteria in the trophosome are retained inside bacteriocytes, thereby having no contact with the external environment. Thus, they rely on Riftia 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 vestimentiferan 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 Riftia pachyptila came from microscopic and biochemical analyses showing Gram negative bacteria packed within a highly vascularized organ in the tubeworm trunk called the trophosome.[21] Additional analyses involving stable isotope,[33] enzymatic,[34][26] and physiological[35] characterizations herbely confirmed that the end symbionts of R. pachyptila oxidize reduced-sulfur compounds in order 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 besides to its entire dependency on its symbionts for nutrition, the bacterial population is thus, the primary source of carbon acquisition for the symbiosis. Discovery of bacterial–invertebrate chemoautotrophic symbioses, initially in vestimentiferan tubeworms[21][26] and then in vesicomyid clams and mytilid mussels,[26] pointed to an even more remarkable source of nutrition sustaining the conspicuous biomass of invertebrates at vents.

Endosymbiosis with Thioautotrophic Bacteria

There is a wide range of bacterial diversity associated with symbiotic relationships with Riftia pachyptila. Many bacteria belong to the class Epsilonproteobacteria[36] as supported by the recent discovery 2016 of the new species Sulfurovum riftiae belonging to the class Epsilonproteobacteria, family Helicobacteraceae isolated from Riftia pachyptila collected from the East Pacific Rise.[37] Other symbionts belong to the class Delta-, Alpha- and Gamma- proteobacteria.[36] The Candidatus Endoriftia persephone is a facultative Riftia 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. It appears that the bacteria prefers a heterotrophic lifestyle when carbon sources are available.[31]

Evidences based on 16S rRNA analysis affirm that R. pachyptila chemoautotrophic bacteria belong to two different phyla of Proteobacteria superphylum: Gammaproteobacteria phylum [38][20] and Epsilonproteobacteria phylum (e.g. Sulfurovum riftiae)[37] that get energy from the oxidation of inorganic sulfur compounds such as hydrogen sulfide (H2S, HS-, S2-) in order to synthetize ATP for carbon fixation via Calvin cycle.[20] 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 a lot of organic matter from them. Thus, because of lack of digestive system, Riftia depends entirely on its bacterial symbiont in order to survive.[39][40]

In the first step of sulfide-oxidation, reduced sulfur (HS-) passes from the external environment into R. pachyptila blood, where, together with O2, it's bound by hemoglobin forming the complex Hb-O2-HS- and then it's transported to the trophosome, where bacterial symbiont resides. Here, HS- is oxidized to elemental sulfur (S0) or to sulfite (SO32-).[20]

In the second step, the symbiont makes sulfite-oxidation thanks to "APS pathway", in order 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 (SO42-) as end products.[20] In formulas:

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 (PRK) and RubisCO.[26][41]

To support this unusual metabolism, Riftia pachyptila has to assume all the substances necessary for both sulfide-oxidation and carbon fixation that is: HS-, O2 and CO2 and other fundamental bacterial nutrients like 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 in Riftia pachyptila

Unlike metazoans, who respire carbone dioxide as a waste product, Riftia-symbiont association has a demand for a net uptake of CO2 instead, as a cnidarian-symbiont associations.[42] 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 2 orders of magnitude greater than the pCO2 of deep-sea water.[42]

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.[20] 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.[43][20] 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.[30]

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.[30][44] 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 24h, labeled carbon is clearely relevant 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.[44][45]

Sulfide acquisition

In deep-sea hydrothermal vents, sulfide and oxygen are present in different areas. Indeed, vent fluid of hydrothermal vents is rich in sulfide, but poor in oxygen, whereas sea water is rich in oxygen. Moreover, sulfide reacts immediately with oxygen to form sulfur compounds like S2O32- or SO42-, unusable for microbial metabolism.[46] 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.[47][20] In fact, Riftia pachyptila is able to cover the oxic and anoxic areas in order to get both sulfide and oxygen.[48][49][50] Thanks to its hemoglobin that can bind sulfide reversibly and apart from oxygen by means of two cysteine residues,[51][52][53] and then transport it to the trophosome where bacteria metabolism can occur.

Symbiont acquisition

The acquisition of a symbiont by a host can occur in three different ways:

  • by environmental transfer (symbiont acquired from a free-living population in the environment);
  • by vertical transfer (parents transfer symbiont to offspring via eggs);
  • by horizontal transfer (hosts that share the same environment).

Evidences suggest that Riftia pachyptila acquires its symbiont via its environment. In fact, 16S rRNA gene analysis showed that vestimentiferan tubeworms belonging to three different genera: Riftia, Oasisia and Tevnia, share the same bacterial symbiont phylotype.[54][55][56][57][58]

This proves that R. pachyptila takes its symbiont from a free-living bacterial population in the environment. Other studies also support this thesis, because analyzing R. pachyptila eggs there were not found 16S rRNA belonging to the symbiont, showing that the bacterial symbiont is not transmitted via vertical transfer.[59]

Another proof to support the environmental transfer comes from several studies conducted in the late 1990s.[60] PCR was used to detect and identify a Riftia pachyptila symbiont gene whose sequence was very similar to the fliC gene which encodes some primary protein subunits (flagellin) required for flagellum synthesis. Analysis showed that R. pachyptila symbiont has at least one gene needed for flagellum synthesis. Hence the question was what the flagellum was for. Flagellar motility would be useless for a bacterial symbiont transmitted vertically, but if the symbiont came from the external environment then a flagellum would be essential to reach the host organism and to colonize it. Indeed, several symbionts use this method to colonize eukaryotic hosts.[61][62][63][64]

Thus, these results confirm the environmental transfer of R. pachyptila symbiont.

Reproduction

Riftia pachyptila (Jones, 1981) [65] is a dioecious vestimentiferan.[66] Individuals of this species are sessile and are found clustered together around deep-sea hydrothermal vents of the East Pacific Rise and the Galapagos Rift.[67] The size of a patch of individuals surrounding a vent is within the scale of tens of metres.[68]

The male's spermatozoa are thread shaped and are composed of three distinct regions: the acrosome (6 μm), the nucleus(26 μm) and the tail (98 μm). Thus, the single spermatozoa is long circa 130 μm overall, with a diameter of 0.7 μm which becomes narrower near the tail area, reaching 0.2 μm. The sperm is arranged into an agglomeration of around 340-350 individual spermatozoa that create a torch-like shape. The cup part is made up of acrosomes and nucleus while the handle is made up by the tails. The spermatozoa in the package are held together by fibrils. Fibrils also coat the package itself to ensure cohesion.

The large ovaries of females run wihin the gonocoel along the entire length of the trunk and are ventral to the trophosome. Eggs at different maturation stages can be found in the middle area of the ovaries and, depending on their developmental stage, are referred to as: oogonia, oocytes and follicular cells. When the ocytes mature they acquire protein and lipid yolk granules.

Males release their sperm into sea water. While the released agglomeration of spermatozoa, referred to as spermatozeugmata, does not remain intact for more than 30 seconds in laboratory conditions, it has been suggested that it may maintain integrity for longer periods of time in specific hydrothermal vent conditions. Usually the spermatozeugmata swims into the female's tube. Movement of the cluster is conferred by the collective action of each spermatozoon moving independently. Reproduction has also been observed involving only a single spermatozoon reaching the female's tube. Generally fertilization in R. pachyptila is considered internal. However, some argue that, as the sperm is released into sea water and only afterwards reaches the eggs in the oviducts, it should be defined as internal-external.

Riftia pachyptila is completely dependent on the production of vulcanic gases and the presence of sulfide-oxidizing bacteria. Therefore, its metapopulation distribution is profoundly linked to vulcanic and tectonic activity that create active hydrothermal vent sites with a patchy and ephemeral distribution. The distance between active sites along a rift or adjacent segments can be very high, reaching 100s of km.[67] This raises the question regarding larval dispersal. R. pachytpila is capable of larval dispersal across distances of 100 to 200 km[67] and cultured larvae show to be viable for a time span of 38 days.[69] However, even though dispersal is considered to be effective, the genetic variability observed in R. pachyptila metapopulation is low compared to other vent species. This may be due to high extinction events and colonization events, as R. pachyptila is one of the first species to colonize a new active site.[67]

The endosymbionts of R. pachyptila are not passed to the fertilized eggs during spawning but are acquired later during the larval stage of the vestimentiferan worm. R. pachyptila planktonic larvae that are trasported through sea-bottom currents until they reach active hydrothermal vents sites, are referred to as trophocores. The trophocore stage lacks endosymbionts, which are acquired once larvae settle in a suitable environment and substrate. Free-living bacteria found in the water column are ingested randomly and enter the worm through a ciliated opening of the branchial plume. This opening is connected to the trophosome through a duct that passes through the brain. Once the bacteria are in the gut, the ones that are beneficial to the individual, namely sulfide- oxidizing strains are paghocytized by epithelial cells found in the midgut and are therefore retained. Bacteria that do not represent possible endosymbionts are digested. This raises questions as to how R. pachyptila manages to discern between essential and non-essential bacterial strains. The worm's ability to recognise a beneficial strain as well as preferential host-specific infection by bacteria have been both suggested as being the drivers of this phenomenon.[70]

Growth rate and age

Riftia pachyptila has the fastest growth rate of any known marine invertebrate. These organisms have been known to colonize a new site, grow to sexual maturity and increase in length to 4.9 feet (1.5 m) in less than two years.[71]

Because of the peculiar environment in which R.pachyptila thrives, this species differes greatly from other deep-sea species that do not inhabit hydrothermal vents sites: the activity of diagnostic enzymes for glycolisis, citric acid cycle and transport of electrons in the tissues of R.pachyptila is very similar to the activity of these enzymes in the tissues of shallow-living animals. This contrasts with the fact that deep-sea species usually show very low metabolic rates. This suggests that low water temperature and high pressure in the deep sea do not necessarily limit the metabolic rate of animals and that hydrothermal vents sites display characteristics that are completely different to the surrounding environment, thereby shaping the physiology and biological interactions of the organisms living in these sites.[32]

Curiosity
  1. The association between Riftia pachyptila and its symbiont was the first symbiosis described for a marine invertebrate and chemoautotrophic bacteria.[21]
  2. Riftia pachyptila has very high growth rates, in fact it is estimated an increase of up 1.4% of its organic carbon per day.[72][71]

See also

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