Giant tube worm

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Giant tubeworm
Scientific classification Edit this classification
Kingdom: Animalia
Phylum: Annelida
Clade: Pleistoannelida
Clade: Sedentaria
Order: Sabellida
Family: Siboglinidae
Genus: Riftia
M. L. Jones, 1981
Species:
R. pachyptila
Binomial name
Riftia pachyptila
M. L. Jones, 1981

Riftia is a monotypic genus of polychaete annelid worms in the Siboglinidae familiy,[1] which contains the sole species Riftia pachyptila, commonly known as the giant tubeworm or giant beardworm.

Unlike other polychaete tube worms found in shallow water marine environments, R. pachyptila lives in association with geologically active regions of the deep sea. Individuals can reach a length of 3 m (9 ft 10 in),[2] and aggregate in large colonies around hydrothermal vents, which provide a natural ambient temperature ranging from 2–30 degrees Celsius (36–86 °F)[3] and emit large amounts of chemicals such as hydrogen sulfide. Adult Riftia worms lack a digestive system and rely on their symbiotic relationship with chemotrophic sulfur-oxidising bacteria to provide them with energy.

Historically, the genus Riftia was placed within the phyla Pogonophora and Vestimentifera.

Discovery

DSV Alvin, US Navy research submarine

R. pachyptila was discovered in 1977 during an expedition led by geologist Jack Corliss to the Galápagos Rift; the survey was sponsored by the Woods Hole Oceanographic Institution and the National Science Foundation, and the dive was carried out by the American bathyscaphe DSV Alvin. The presence of thermal springs near mid-oceanic ridges was presumed, and the expedition aimed to confirm this.[4]

The discovery of life around hydrothermal vents was unexpected. The vents were assumed to be sterile environments due to high heat emitted from them (around 350–380 °C (662–716 °F)),[5][6] thus no biologists were included in the expedition. Many of the species discovered during this expedition had never been seen before, as they are found exclusively near hydrothermal vents. Observed species included "foot-long" bivalves (the mussel Bathymodiolus thermophilus and clam Calyptogena magnifica), white crabs, and polychaetes such as R. pachyptila.[7] The discovery was compared to that of Columbus' discovery of the Americas by one of the geologists.[4][8] Hydrothermal activity at this site was determined to have begun during the early 1970s, with the tubeworms ecologically dominating the site prior to 1979.[9]

Though initially thought to be an isolated phenomenon, this vent ecosystem (located at 00°48′15″N 86°13′29″W / 0.80417°N 86.22472°W / 0.80417; -86.22472;[10] dubbed the "Rose garden" site due to the prevalence of the red Riftia worms)[4] proved to be the first of many such ecosystems that would later be discovered on other geologically active sections of the sea floor. An expedition in 1985 returned to the Rose Garden site and found that the Riftia were fewer in number, having been displaced by clams and mussels despite having "essentially the same" water chemistry as the initial discovery in 1979.[9] Another returning expedition in 2002 found that it had been destroyed by a lava flow sometime in the prior decade, though a second vent ecosystem was found near the original site, which it was dubbed "Rosebud".[4]

Description

The generic name Riftia alludes to the rift that formed the geothermal vents where the species inhabits, while pachyptila (pachy; thick + ptilon; feather) refers to the anterior plume of the worm.[10] The original specimen or holotype, USNM 59951, is held by the National Museum of Natural History (USNM).[4]

Anatomy

Tubes

Being extracted out of its tube

Riftia's tubes are composed of chitin associated with proteins,[11] which are secreted out from cup-shaped microvilli-like structures within glands which form crystallite chitin layers over time.[12] Their tubes are very thick compared to cold-seep tubeworms and pogonophorans, especially at the base.[13] These tubes are very resistant to enzymatic attack by bacteria, and can take years to decompose.[14]The worms are able to remodel both the top and the base of their tubes, which allows for some adaptability in the highly competitive and crowded spaces they grow in- a worm may need to adjust its position to maximise its access to vent fluid as more worms settle in the colony.[15] Growth rate of the tubes range from 10 to 85 cm (3.9 to 33.5 in) per year.[16][17] The amount of chitin produced approaches 100 times that of pelagic and benthic ecosystems.[12]

Body

Riftia tube worms can reach a length of 3 m (9 ft 10 in),[2] and their bodies have a diameter of 4 cm (1.6 in).

R. pachyptila community with extroflexion of red branchial plume

Inside the tube, R. pachyptila has a vermiform body topped with a bright red feather-like structure called a branchial plume, which is used to acquire chemicals for chemosynthesis. The plume is highly vascularised, and its colour is due to the presence of hemoglobin that contains up to 144 globin chains. Tube worm hemoglobins are atypical in that they are able to carry oxygen in the presence of sulfide without being inhibited by it.[18][19] Hemoglobins in the branchial plume are able to bind O2 and H2S, which are necessary for chemosynthetic bacteria inside the trophosome. Capillaries in the branchial plume move these compounds to the trophosome, where they can be absorbed by bacteria.[20] After Paralvinella grasslei, Riftia has the second highest branchial surface area among aquatic animals, having 11.6–30.9 cm2 (1.80–4.79 sq in) of branchial area per gram of wet mass (with the sampled worms ranging from 0.9 to 112.3 g (0.032 to 3.961 oz)). Larger, typically mature worms have proportionally smaller branchial areas compared to smaller immature ones.[13] If the tubeworm perceives a threat or is touched, it retracts the plume into its tube and seals the tube with its obturaculum, a kind of operculum.[21] The collagenous obturaculum supports the respiratory lamellae.[22]

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.[23][24] The heart, extended portion of dorsal vessel, enclose the vestimentum.[25]

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 also located the trophosome, a spongy tissue where a billion symbiotic, thioautotrophic bacteria and sulfur granules are found.[26][27] Since the mouth, digestive system, and anus are missing, the survival of R. pachyptila is dependent on this mutualistic symbiosis.[28] This process, known as chemosynthesis, was recognized within the trophosome by Colleen Cavanaugh.[28]

In the posterior part, the fourth body region, is the opisthosome, which anchors the animal to the tube and is used for the storage of waste from bacterial reactions.[29]

Physiology

Anatomy of Riftia pachyptila, including microstructure and metabolic process

Metabolism

Due to its highly specific hydrothermal vent habitat, 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.[30]

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

Relationship with endosymbiotic bacteria

In its adult phase, R. pachyptila lacks a digestive system and cannot eat. Rather than consuming organic matter, 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 (coelom).[28] These bacteria are able to convert common chemicals in the hydrothermal vent environment into carbohydrates that can be consumed by the tube worm.[27][31][32] These chemicals typically include carbon, nitrogen, oxygen, and sulfur, which are absorbed by the tube worm into its trophosome to provide the bacteria with nutrition.

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). In turn, the tube worm depends completely on the bacteria for the carbohydrate byproducts of the carbon fixation cycles that the bacteria performs when supplied with such nutrients. These carbohydrates provide the tube worm with nutrition.

Bacterial carbon fixation process

The bacteria that live in symbiosis with Riftia tubeworms are chemotrophic organisms that obtain energy from the oxidation of chemicals in their environment, as opposed to photosynthetic organisms that capture photons to acquire energy. This allows the bacteria to live in habitats such as deep ocean vents with no sunlight. Bacteria that live in symbiosis with Riftia utilise sulfides for this oxidation in a process referred to as thioautotrophy.

The host tubeworm intakes the chemicals required for thioautotrophy (HS−, O2, and CO2) from the mineral-rich vent environment and transports them to the bacteria within its trophosome, which retains a large number of bacteria on the order of 109 bacteria per gram of fresh weight.[30] These bacterial symbionts then oxidise sulphur compounds to synthesise ATP for use in autotrophic carbon fixation through the Calvin cycle. [33][34][35][36] The tubeworm then receives back a portion of the organic matter synthesized by the symbiont population. The adult tubeworm is unable to feed on particulate matter and depends on its symbionts for nutrition. The bacterial population is then the primary source of carbon acquisition for the symbiosis.

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 (SO32-).[27]

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 (SO42-) as end products.[27] In formulas:

  • AMP + SO 3 2 − → A P S r e d u c t a s e APS {\displaystyle {\ce {AMP + SO3^2- ->[APSreductase] APS}}} {\displaystyle {\mathrm {AMP} {}+{}\mathrm {SO} {\vphantom {A}}_{\smash[{t}]{3}}{\vphantom {A}}^{2-}{}\mathrel {\xrightarrow {\mathrm {APSreductase} } } {}\mathrm {APS} }}
  • APS + PPi → A T P s u l f u r y l a s e ATP + SO 4 2 − {\displaystyle {\ce {APS + PPi ->[ATP sulfurylase] ATP + SO4^2-}}} {\displaystyle {\mathrm {APS} {}+{}\mathrm {PPi} {}\mathrel {\xrightarrow {\mathrm {ATP} ~\mathrm {sulfurylase} } } {}\mathrm {ATP} {}+{}\mathrm {SO} {\vphantom {A}}_{\smash[{t}]{4}}{\vphantom {A}}^{2-}}}

The electrons released during the entire sulfide-oxidation process enter in an electron transport chain, yielding a proton gradient that produces ATP (oxidative 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.[35][37]

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 phosphorylation. In R. pachyptila the production of hydrogen sulfide starts after 24h of hypoxia. 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.

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.[19]

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.[38] 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.[38]

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.[27] 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.[39][27] 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.[32]

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.[32][40] 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.[40][41]

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 seawater is richer in dissolved oxygen. Moreover, sulfide is immediately oxidized by dissolved oxygen to form partly, or totally, oxidized sulfur compounds like thiosulfate (S2O32-) and ultimately sulfate (SO42-), respectively less, or no longer, usable for microbial oxidation metabolism.[42] This causes the substrates to be less available for microbial activity, thus bacteria are constricted to compete with oxygen to get their nutrients. To avoid this issue, several microbes have evolved to make symbiosis with eukaryotic hosts.[43][27] In fact, R. pachyptila is able to cover the oxic and anoxic areas to get both sulfide and oxygen[44][45][46] thanks to its hemoglobin that can bind sulfide reversibly and apart from oxygen by functional binding sites determined to be zinc ions embedded in the A2 chains of the hemoglobins.[47][48][49] and then transport it to the trophosome, where bacterial metabolism can occur. It has also been suggested that cysteine residues are involved in this process.[50][51][52]

During the chemosynthesis, the mitochondrial enzyme rhodanase catalyzes the disproportionation reaction of the thiosulfate anion S2O32- to sulfur S and sulfite SO32- .[53][54] The R. pachyptila's bloodstream is responsible for absorption of the O2 and nutrients such as carbohydrates.

Endosymbiont species

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.[28]

A wide range of bacterial diversity is associated with symbiotic relationships with R. pachyptila. Many of these bacteria belong to the phylum Campylobacterota[55] as supported by the recent discovery in 2016 of the new species Sulfurovum riftiae collected from the East Pacific Rise.[56] Other symbionts belong to the classes Delta-, Alpha- and Gammaproteobacteria.[55]

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.[57]

Evidence based on 16S rRNA analysis affirms that R. pachyptila chemoautotrophic bacteria belong to two different clades: Gammaproteobacteria[58][27] and Campylobacterota (e.g. Sulfurovum riftiae)[56] that get energy from the oxidation of inorganic sulfur compounds such as hydrogen sulfide (H2S, HS−, S2-) to synthesize ATP for carbon fixation via the Calvin cycle.[27] 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 a lack of a digestive system, R. pachyptila depends entirely on its bacterial symbiont to survive.[59][60]

Biology

Riftia tubes covered in epibionts
Alongside mussels and sea anemones

Riftia pachyptila are sessile and are found clustered together around deep-sea hydrothermal vents of the East Pacific Rise and the Galapagos Rift.[61] The size of a patch of individuals surrounding a vent can span tens of metres.[62] R. 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 ft (1.5 m) in less than two years.[63]

Study of the Rose Garden site determined that the three species of major sessile animals present have different microhabitat requirements;[9] that is to say, they are able to coexist at the same sites through niche partitioning. Riftia apparently 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.[9] The Rose Garden was estimated to have become hydrothermically active in the early 70s, and while Riftia and the two bivalve species probably colonized the site shortly after, Riftia's greater "autotrophic potential" allowed them to grow faster and dominate the site before the 1979 observation. Between 1979 and 1985, the more opportunistic mussels reached their maximum sizes, and their dense growth on Riftia tubes altered the local microhabitat; vent flows were diverted away from the tubeworm's plumes and mussel growth may have interfered with the growth of smaller Riftia worms. As a result, the tubeworms dominance over the site subsided, with the bivalves displacing the tubeworms as the ecosystem matured with a stable hydrothermal flow, and the two species are thought to persist for "much longer" than the tubeworms if the flow gradually declined.[9]

It is suggested that the smaller-bodied tubeworm Tevnia may facilitate later vent colonization by Riftia.[64][65]

Reproduction

R. pachyptila is dioecious, having two sexes.[66][67] 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 spermatozoon is about 130 μm long 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 form 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 within 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 oocytes mature, they acquire protein and lipid yolk granules.

Males release their sperm into seawater. While the released agglomerations of spermatozoa, referred to as spermatozeugmata, do not remain intact for more than 30 seconds in laboratory conditions, they may maintain integrity for longer periods of time in specific hydrothermal vent conditions. 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. Generally, fertilization in R. pachyptila is considered internal. However, some argue that, as the sperm is released into seawater and only afterwards reaches the eggs in the oviducts, it should be defined as internal-external.

R. pachyptila develops from a free-swimming, pelagic, non-symbiotic trochophore larva, which enters juvenile (metatrochophore) development, becoming sessile, and subsequently acquiring symbiotic bacteria.[68][69] 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 similar to an infection. The digestive tract is transiently connected 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 remodeling and enlargement to become the trophosome, while the remainder of the digestive tract has not been detected in adult specimens.[70]

R. pachyptila is completely dependent on the production of volcanic gases and the presence of sulfide-oxidizing bacteria. Therefore, its metapopulation distribution is profoundly linked to volcanic and tectonic activity that creates 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 hundreds of km.[61] This raises the question regarding larval dispersal. R. pachytpila is capable of larval dispersal across distances of 100 to 200 km[61] and cultured larvae have been shown to be viable for 38 days.[71][72] 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.[61]

Some sources list Riftia pachyptila as one of the world's longest living organisms,[73] but the unstable vent environment and high ecological turnover makes this claim unlikely.[74] 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.[75][76][77][78]

Symbiont acquisition

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 are transported 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 phaghocytized by epithelial cells found in the midgut are then retained. Bacteria that do not represent possible endosymbionts are digested. This raises questions as to how R. pachyptila manages to discern between essential and nonessential 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]

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

  • Environmental transfer (symbiont acquired from a free-living population in the environment)
  • Vertical transfer (parents transfer symbiont to offspring via eggs)
  • Horizontal transfer (hosts that share the same environment)

Evidence suggests that R. pachyptila acquires its symbionts through 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.[79][80][81][82][83]

This proves that R. pachyptila takes its symbionts from a free-living bacterial population in the environment. Other studies also support this thesis, because analyzing R. pachyptila eggs, 16S rRNA belonging to the symbiont was not found, showing that the bacterial symbiont is not transmitted by vertical transfer.[84]

Another proof to support the environmental transfer comes from several studies conducted in the late 1990s.[85] PCR was used to detect and identify a R. pachyptila symbiont gene whose sequence was very similar to the fliC gene that 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 arose as to the purpose of the flagellum. 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.[86][87][88][89]

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


See also

References

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