Riftia

Anatomy

Like other siboglinade tube worms, R. pachyptila has a vermiform body that secretes a chitinous tube for protection and support.^[9] Riftia worms can reach a length of 3 m (9 ft 10 in),^[3] and their bodies have a diameter of 4 cm (1.6 in).

Riftia have a red feather-like structure called a branchial plume at the anterior end which is used to acquire chemicals for chemosynthesis. The plume is highly vascularised, and its red colour is due to the presence of hemoglobin. The structure of the plume maximises the surface area needed to absorb chemicals from the water efficiently. If the tubeworm perceives a threat or is touched, it retracts the plume into its tube and seals the tube with its obturaculum, an operculum made of collegen.^[10] The respiratory lamellae are supported by the obturaculum.^[11]

Beneath the plume is the vestimentum, a muscular body region that contains the heart and the two genital openings.^[12][13][14]

The middle region of the body houses the coelomic cavity, gonads, and the trophosome, a spongy tissue where symbiotic bacteria and sulfur granules are found.^[15][16] Adult Riftia have no mouth, digestive system or anus as they do not eat. Instead, they rely on bacteria in their trophosome to provide them with nutrition.^[17]

The posterior part of the worm is the opisthosome, which anchors the animal to the tube and is used for the storage of waste from bacterial reactions.^[18]

Tubes

Riftia's tubes are composed of chitin,^[19] secreted out from cup-microvilli-like structures within glands which form crystallite chitin layers over time.^[20] The tube is cylindrical, flexible, and closed at the prosterier end.^[21] Riftia tubes can reach 2 m in length and 5 cm in diameter and are very thick compared to those of other tubeworms, especially at the base.^[22][6] The tubes are very resistant to enzymatic attack by bacteria, and can take years to decompose.^[23] The worms are able to adjust both the top and the base of their tubes, which allows for some adaptability in the highly competitive and crowded spaces they grow in, as a worm may need to adjust its position to maximise its access to vent fluid as more worms settle in the colony.^[24] Riftia tubes grow at a rate of 10 to 85 cm (3.9 to 33.5 in) per year.^[25][26]

Metabolism

R. pachyptila differs significantly in its physiology from other deep-sea species that do not inhabit hydrothermal vent sites. While deep sea species typically have low metabolic rates, the enzyme activity relating to glycolysis, the citric acid cycle and electron transport in the tissues of R. pachyptila is similar to that of shallow-living animals, suggesting a significantly faster metabolism than is typical of species found in the deep sea.^[27] In order to support their metabolism, R. pachyptila has to absorb all the substances necessary for both sulfide-oxidation and carbon fixation as well as other fundamental bacterial nutrients such as nitrogen and phosphorus. 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 than the surrounding water. The exact mechanism of R. pachyptila's ability to withstand and concentrate nitrate is still unknown.^[28]

Hydrothermal vents produce conditions of high hypoxia. In hypoxic conditions, sulfur-storing organisms start producing hydrogen sulfide. In R. pachyptila the production of hydrogen sulfide starts after 24h of hypoxia. H₂S can be damaging for some physiological processes as it inhibits the activity of cytochrome c oxidase, impairing oxidative phosphorylation. To avoid physiological damage Riftia pachyptila are able to bind H₂S to haemoglobin in the blood to expel it in the surrounding environment.

Relationship with endosymbiotic bacteria

In its adult phase, R. pachyptila lacks a digestive system and cannot eat. Instead, Riftia gains nutrients from the environment by utilising a process known as chemoautotrophic symbiosis.

In this process, nutrition is gained via sulfur-oxidizing endosymbiotic bacteria that live in a specialised organ inside the worm called the trophosome, a soft tissue that runs almost the whole length of the tube worm's body cavity.^[17] These bacteria are able to convert common chemicals in the hydrothermal vent environment into carbohydrates that can be consumed by the tube worm.^[16][29][30] These chemicals typically include carbon, nitrogen, oxygen, and sulfur, which are transported by the tube worm into its trophosome to provide the bacteria with nutrition. Riftia acquires nutrients from the bacteria by digesting part of the symbiont population.^[31]

Riftia hemoglobins are atypical in that they are able to carry oxygen in the presence of sulfide without being inhibited by it.^[32][28] Hemoglobins in the branchial plume are able to bind O₂ and H₂S, which are necessary for bacterial chemosynthesis. Capillaries in the branchial plume move these compounds to the trophosome, where they can be absorbed by bacteria.^[33] Bacteria in the trophosome live inside specialised cells (bacteriocytes) and have no contact with the external environment, relying entirely on the tube worm for nutrients as well as for the removal of its waste products (carbohydrates).

Ecology

Riftia is able to coexist with other large sessile animals through niche partitioning.^[34] Riftia requires areas of high water flow, temperature, and sulfide concentrations, in contrast to Calyptogena magnifica's need of low flow and temperature, and Bathymodiolus thermophilus' flexibility; B. thermophilus mussels may grow in places ranging from the periphery of the vent field, to directly on Riftia's tubes.^[34]

It is suggested that the smaller-bodied tubeworm Tevnia may facilitate later vent colonization by Riftia.^[35][36]

Reproduction

R. pachyptila is dioecious.^[37][38] The male's spermatozoa are thread-shaped and are about 130 μm long overall. The sperm is arranged into an agglomeration of around 340–350 individual spermatozoa that form a torch-like shape, referred to as spermatozeugmata. ^{[citation needed]}

The ovaries of females run within the gonocoel along the entire length of the trunk, 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 oocytes mature, they acquire protein and lipid yolk granules.^{[citation needed]}

Males release their sperm into seawater. Usually, the spermatozeugmata swim 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. ^{[citation needed]}

Larval stage

R. pachyptila develops from a free-swimming, pelagic, non-symbiotic trochophore larva, which enters juvenile (metatrochophore) development, becoming sessile, and subsequently acquiring symbiotic bacteria.^[39][40] R. pachyptila larvae are planktonic and move through sea-bottom currents until they reach active hydrothermal vent sites.

The digestive tract is present in the larval stage and consists of a mouth foregut, midgut, hindgut, and anus. After symbionts are established in the midgut, they undergo substantial remodeling and enlargement to become the trophosome, while the remainder of the digestive tract has not been detected in adult specimens.^[41]

R. pachyptila is dependent on volcanic gases and the presence of sulfide-oxidizing bacteria. It acquires these from hydrothermal vent sites that are patchy and ephemeral. The distance between active sites along a rift can be hundreds of km.^[2] R. pachytpila is capable of larval dispersal across distances of 100 to 200 km^[2] and cultured larvae have been shown to be viable for 38 days.^[42][43] 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.^[2]

Lifespan

Some sources list Riftia pachyptila as one of the world's longest living organisms,^[44] but the unstable vent environment and high ecological turnover makes this claim unlikely.^[45] Tube worms inhabiting stable cold seep environments such as Lamellibranchia and Escarpia have better claims to longevity, with age measurements of both species exceeding a century.^{[46][47][48][49]}

Background

Most ecosystems on earth rely on photosynthetic organisms, such as plants to form the base of their food web. Photosynthetic organisms use light energy from sunlight to convert carbon dioxide and water into carbohydrates and oxygen. The carbohydrates produced provide energy to the organisms, as well as to other organisms higher up in the food chain that consume them.

However, in deep sea environments no sunlight is able to reach the sea floor, and photosynthesis becomes impossible. Hydrothermal vent ecosystems are instead based on chemosynthetic microbes such as sulfur-oxidising bacteria. These microbes are able to generate carbohydrates utilising the energy released from chemical reactions in the same way that photosynthetic organisms utilise light energy. The carbohydrates produced by chemosynthetic microbes can then be consumed by other organisms, forming the basis of the hydrothermal vent food chain.

Different kinds of chemotropic organisms specialise in consuming particular chemicals. The bacteria that live in symbiosis with Riftia are sulfur-oxidising chemotrophs that utilise sulfides in their chemosynthesis. This form of chemosynthesis is referred to as thioautotrophy.^{[18][better source needed]}

Bacterial symbiosis

Riftia worms live in symbiosis with the sulfur-oxidising bacteria inside their trophosome. The tube worm provides the bacteria with the chemicals required for chemosynthesis, and the bacteria are a source of carbon that can be consumed by the tube worm.^[50]

Process of thioautotrophic chemosynthesis

Riftia worms take in hydrogen sulfide, carbon dioxide, and oxygen from the mineral-rich vent environment through their plume. These chemicals pass into the tube worm's blood, where they are bound by hemoglobin and transported to the trophosome. The bacterial symbionts then utilise these chemicals to perform chemosynthesis.^[16] The simplified chemical equation for this process is:

CO₂carbon
dioxide + 4H₂Shydrogen
sulfide +O₂oxygen→CH₂Ocarbohydrate+ 4Ssulfur + 3H₂Owater^[50]

Because R. pachyptila must uptake CO_2. for its metabolism, CO₂ uptake in the worm is enhanced by the higher pH of its blood (7.3–7.4), which favors the bicarbonate ion and promotes a steep gradient across which CO₂ diffuses into the vascular blood of the plume.^[56][16][57]

Once the CO₂ is fixed by the symbionts, it can be consumed by the host tissues. The fixed carbon is transported via organic molecules from the trophosome in the hemolymph.^[30][58]