siboglinid tube worm and bacteria relationship
A crucial adaptation in the evolution of siboglinids appears to be a unique circulatory system that allows these chemicals to be delivered to the symbionts. Notwithstanding possible exceptions, the overall rank order of fecundity and dispersal distance of siboglinids is: Vestimentifera>Osedax>Frenulata corresponding to the degree of transience and isolation of the habitats occupied by these groups. Or are they a more recently-evolved branch of the tree of life, derived from more conventional filter-feeding polychaetes with which they share several morphological similarities? Muller's ratchet phenomenon, together with less effective population sizes, leads to an accretion of deleterious mutations in the non-essential genes of the intracellular bacteria. Dorland's Illustrated Medical Dictionary. The three frenulate species examined to date harbour primary endosymbionts within a monophyletic clade of thiotrophic Leucothrix-Methylococcaceae Gammaproteobacteria –. Four major groups of siboglinids are … For example, in lichens, which consist of fungal and photosynthetic symbionts, the fungal partners cannot live on their own. The first attempt to age the Siboglinidae based on genetic data suggested a relatively recent Mesozoic or Cenozoic origin . Examples of metabiosis are hermit crabs using gastropod shells to protect their bodies, and spiders building their webs on plants. They found that two species of tube worms actually trap methane, a powerful greenhouse gas, through a never-before-seen symbiotic relationship between the worms and methane-eating bacteria. Tube worms are resistant to great heat. Was it driven by the geological formation of spreading centres and hydrocarbon seeps? , As the endosymbiont adapts to the host's lifestyle, the endosymbiont changes dramatically.  There are two types of amensalism, competition and antagonism (or antibiosis). The obligate symbiosis in siboglinid tubeworms at deep-sea vents, seeps and whale-falls is a most remarkable biological adaptation. Furthermore, the discovery of unexpectedly different metabolic types of symbionts, with putatively heterotrophic metabolism opposed to chemoautotrophy, in the Osedax clade  and potential symbiont diversity in other gutless worms  has illustrated that much knowledge of the diversity and function of these relationships awaits discovery. The trophosome of this beard worm harbors sulfur-oxidizing bacteria. Symbiosis is also classified by physical attachment. Only a small fraction of the global ridge system (∼65 000 km) and of the vast continental margin regions have been explored. The complex taxonomic story of the siboglinids has been recently well reviewed , – and is, as Rouse  stated “one of the more fascinating tales in animal systematics.” In the days prior to robust cladistic analysis or molecular evidence, a long scientific debate was held as to the possible origins of these enigmatic worms. Under much controversy , Riftia pachyptila was elevated to phylum ‘status’  under the name Vestimentifera. . Although sulphide binding has not been demonstrated for the ring-Hb, it has an extremely high affinity for oxygen , ,  that enables the worm to take up and transport large amounts of oxygen while maintaining low internal dissolved O2. relationships between siboglinids and their endosymbiotic bacteria. In vestimentiferans and Sclerolinum specifically, primary endosymbionts are two closely-related clades of chemoautotrophic bacteria within the Leucothrix-Methylococcaceae cluster. By contrast, many vestimentiferan tubes are large (up to 40 mm in diameter) and robust, often having thick tube walls. Furthermore, vestimentiferans mostly live in environments where rapid mineralization occurs, including carbonates at seeps and sulphides at vents. In contrast, if the symbiont is using the host as a resource and causing it harm as a result, then it qualifies as a parasite. Whilst Siboglinidae as a clade of annelid worms is now well accepted, this improvement in the taxonomic situation has done little to help answer our primary question – when did siboglinids evolve? Equally important to adaptations within the circulatory system are the bacterial endosymbionts that are thought to provide the majority of energy to the hosts. The bacteria actually convert the chemicals from the hydrothermal vents into organic molecules that provide food for the worm. It is derived from the English word commensal, used of human social interaction. However, the presence of sabellimorph, tube-dwelling polychaetes in the fossil record does little to help narrow the window of geological history during which Siboglinidae may have evolved. Only molecular genetics have provided recent convincing, consistent character sets, although with hindsight, the morphological clues were always there. Modern systematics can provide preliminary answers to this difficult question. the bacteria oxidize hydrogen sulfide or methane for the worm. broad scope, and wide readership – a perfect fit for your research every time. Web. Siboglinid worms are a group of gutless marine annelids that are nutritionally dependent upon endosymbiotic bacteria. The incapability of the endosymbiotic bacteria to reinstate their wild type phenotype via a recombination process is called Muller's ratchet phenomenon. Given that there are, so far, only four known lineages of siboglinids and that symbionts within a major host lineage seem to be related, there are a limited number of alternative scenarios for the evolutionary origins of this symbiosis. The hydrothermal vent habitat of many vestimentiferans is often characterised as an ‘extreme environment’, where organisms must live on the side of mineralized hydrothermal chimneys in which hydrogen sulphide enriched fluids emanate at temperatures of up to 400°C. Although no estimates exist for larval dispersal distances and duration of Frenulata, it is known that some species incubate eggs in their tubes until settlement stage (Figure 7c) whereas others have planktonic larvae, although the latter have never been reared . Molecular clocks for Siboglinidae can, in some instances, be calibrated as hydrothermal vent species are intrinsically linked with geology as mid-ocean ridges form and separate. Unfortunately, symbiosis has only been investigated in a handful of siboglinid species. sulphide concentration  or bone degradation stage ). here. Molecular genetics can help. In general the fossil record of these animals is poor, with the main exception being the calcareous tube-forming Serpulidae, which have a slightly better fossil record dating back to the Late Triassic . the Silurian [∼440 Ma] Yamankasia rifeia and Devonian [∼393 Ma] Tevidestus serriformis) are large (up to 39 mm in diameter) external moulds formed by thin layers of pyrite, often preserving fine details of the external tube wall, including faint longitudinal striations, concentric growth lines and flanges . A) Riftia pachyptila giant tubeworms growing on a hydrothermal vent in the north-east Pacific (Image courtesy of Richard Lutz), B) Lamellibrachia luymesi at a cold seep in the Gulf of Mexico (Image courtesy of DT, KH, Kevin Fielman and Scott Santos) and C) Osedax mucofloris living on a whale-bone found off the coast of Sweden. Bacterial symbionts then fix CO2 into organic molecules using sulphide as the energy source , . At cold seeps, siboglinids are almost always living within a sedimented environment, although hard substrates do form through carbonate precipitation. Habitat availability and stability are not, in general, a problem for organisms that can live on approximately 60% of the planet's surface.  When one organism lives on the surface of another, such as head lice on humans, it is called ectosymbiosis; when one partner lives inside the tissues of another, such as Symbiodinium within coral, it is termed endosymbiosis. Given the known diversity of siboglinds, one obvious issue in the study of siboglinid history is the lack of sampling among frenulate taxa. Although support for placement within current classifications is weak , current evidence suggests that Siboglinidae are likely affiliated with the Oweniidae within a clade of ‘sabellimorph’ species that include the Serpulidae and Sabellidae , . For a time, the vestimentiferans were elevated to phylum status , although later studies found close links in the larval development of both Pogonophora and Vestimentifera . To some, these discussions might have appeared as obscure taxonomic arguments of little relevance to modern day issues in biology. mutualism. Wrote the paper: AH MC TGD KMH CTSL DJT CV AGG.  Parasitism takes many forms, from endoparasites that live within the host's body to ectoparasites and parasitic castrators that live on its surface and micropredators like mosquitoes that visit intermittently. The oldest fossil attributed to siboglinids is Hyolithellus micans from the Middle Cambrian (∼500 Ma), based on tube morphology and the probable presence of chitin in the organic component of the tube wall , . It was the formal taxonomic publication, the creation of a compelling name and common language that allowed researchers to finally start linking together work on the biology of these unusual animals. Tubular fossils are also common in Mesozoic and Cenozoic cold seep deposits (, table 1, and references therein), some of which are undoubtedly of serpulid origin. These are the first field photographs of beard worms. The aim of this paper is to address when and how this happened reviewing the available morphological, molecular, environmental and fossil data. Yes Introduction Deep-sea worms in the polychaete family Siboglinidae are not yet thought to be of any commercial or medical value to humans. Females have a transparent mucous tube that encloses the trunk. These taphonomic (i.e. The body can be divided into four main regions: an anterior region, a diaphragm, a trunk region and a segmented opisthosoma. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. One piece of evidence in support of this hypothesis is that vestimentiferans, with thiotrophic symbionts, have been recorded occasionally in sediments containing whalebones, although never ecologically dominant . She considered Darwin's notion of evolution, driven by competition, to be incomplete and claimed that evolution is strongly based on co-operation, interaction, and mutual dependence among organisms. The trophosome (light grey) houses endosymbiotic bacteria (orange ovals). Discover a faster, simpler path to publishing in a high-quality journal. PLoS ONE 6(2): A similar pattern of rapid mineralization of vestimentiferan tubes at seeps is found on the Congo deep-sea fan where some posterior ‘root’ tubes of Escarpia southwardae are partially to completely replaced by the carbonate mineral aragonite , . Tube worms rely on the bacteria in their enviornment to oxidize hydrogen sulfide, using dissolved oxygen in the water as an electron acceptor. Credo Reference. We believe that the exploration of new chemosynthetic environments, on planet earth and perhaps beyond, will include the discovery of new species capable of ecological and physiological attributes that cannot yet be imagined. "symbiosis." Among the many types of mimicry are Batesian and Müllerian, the first involving one-sided exploitation, the second providing mutual benefit. These additional bacterial types consist of multiple bacterial lineages, including Alpha, Gamma, and Epsilonproteobacteria as well as members of the Bacteroidetes (e.g., , , , –). Ectosymbiosis is any symbiotic relationship in which the symbiont lives on the body surface of the host, including the inner surface of the digestive tract or the ducts of exocrine glands. https://doi.org/10.1371/journal.pone.0016309.g004. Yes With the exception of Osedax, the external anatomical characters are relatively constant among all siboglinids. Remarkably, Nussbaumer et al.  Evidence for this includes the fact that mitochondria and chloroplasts divide independently of the cell, and the observation that some organelles seem to have their own genome. Annelida. While difficult logistics have so far precluded intensive time-series studies of the reproductive activity of any siboglinid species, much has been learned about the reproductive ecology through “snap-shot” analyses of, for example, gametogenic condition, population structure and population genetics –. what phylum are peanut worms in? The circular story of Siboglinidae systematics is, as Pleijel et al. The bryozoan colony (Acanthodesia commensale) develops a cirumrotatory growth and offers the crab (Pseudopagurus granulimanus) a helicospiral-tubular extension of its living chamber that initially was situated within a gastropod shell. Thus, the hypothetical thiotrophic Osedax-ancestor made the evolutionary transition to heterotrophy. e16309. In spite of the spectacular discoveries and extraordinary advances made in recent years the placement of siboglinids among the annelid tree is still poorly resolved and many other questions concerning the evolution and ecology of siboglinids remain unanswered. The tubular fossils from the seep deposits (e.g. No, Is the Subject Area "Larvae" applicable to this article? Bronstein, J. L. (2015). , Type of a close and long-term biological interaction between two different biological organisms, This article is about the biological phenomenon. The shrimp digs and cleans up a burrow in the sand in which both the shrimp and the goby fish live. A special mucus on the clownfish protects it from the stinging tentacles. Attached to the name is often a hypothesis of an organism's closest relatives. An ancestor of Osedax may have contained a typical thiotrophic endosymbiont form that utilized sulphide rich sediment around whalebones. ", About 80% of vascular plants worldwide form symbiotic relationships with fungi, in particular in arbuscular mycorrhizas. If correct this would constitute the oldest fossil record of this clade and the age is roughly the same as the first major radiation of whales, which strengthens the idea of an evolutionary link between Osedax and its main modern substrate . 1981 Jul 17; 213 (4505):340–342. At organic-rich sediments, sulphide is produced during the anaerobic degradation of a range of organic compounds. Identical longitudinal ridges can be seen in the tubes of modern vestimentiferan tubes, particularly at the anterior ends, in both vent (Figure 5c) and seep species (e.g., , fig. Similarly, studies of early development based on spawning wild-caught individuals have provided insights into dispersal of all siboglinid clades , , , , . These polychaetes all share a similar sessile, tube-dwelling lifestyle and exhibit less pronounced segmentation and reduced chaetal structures. This is to the advantage of the mimic but to the detriment of both the model, whose protective signals are effectively weakened, and of the dupe, which is deprived of an edible prey. It is rare that deep-sea worm genera such as Riftia or Osedax are described in the pages of Nature or Science.  Most land plants and land ecosystems rely on mutualism between the plants, which fix carbon from the air, and mycorrhyzal fungi, which help in extracting water and minerals from the ground. A taxonomic revision was undertaken  and together with molecular studies , , – the name Siboglinidae is now firmly established as representative of the worms formally known as Vestimentifera and Pogonophora. Recent molecular and morphological studies however, show that Sclerolinum is the sister clade to vestimentiferans , . Credo Reference. The timing (larval or post settlement) and mechanism of symbiont acquisition from the environment are not known for other siboglinid groups. The second body region is responsible for the names Vestimentifera and Frenulata. observ.). Arguably, this single species of worm launched the careers of a generation of deep-sea biologists. A Bayesian analysis of 18S ribosomal RNA sequences reveals four major clades of siboglinids, from top, Osedax which are specialist on whale carcasses, the vestimentiferans, which are specialist on vents and seeps, Sclerolinum (here presented only by a single sequenced specimen), specialist on organic-rich remains and the frenulates which specialise on organic-rich sediments. Considering the diversity of both siboglinid worms and the habitats that they occupy, the existence of considerable bacterial endosymbiont diversity is perhaps unsurprising. In Vestimentifera, the anterior region is called the obturaculum, it functions as an operculum that closes the tube when the animal withdraws, and supports the large branchial plume. Throughout the process, the mature tree is unaffected by the sapling. 17 September 2012.  For example, different species of bumblebee mimic each other, with similar warning coloration in combinations of black, white, red, and yellow, and all of them benefit from the relationship. The term was subject to a century-long debate about whether it should specifically denote mutualism, as in lichens. The discovery of the opisthosome region at the posterior end of the worm, with its clear annelid-like segmentation and serially-arranged chaetae ,  should have been sufficient evidence to place the Pogonophora phylum, as it was then known, within the annelid radiation. Based on molecular genetic and morphological evidence , , we may infer that over evolutionary time conventional heterotrophic polychaetes made the evolutionary leap to specialize as obligate endosymbiotic siboglinid species at chemosynthetic ecosystems. Funding: A. Hilário is supported by a grant (SFRH/BPD/22383/2005) from Fundação para a Ciência e Tecnologia (FCT) and A. Glover by a SynTax grant from the Systematics Association. Apart from one other older estimate (126 mya , ), work in this area has since stalled and more recent studies have focused mainly on direct evidence from fossils. Yes For almost 80 years, from their discovery in 1914 to the first molecular phylogenies in the 1990s, there was disagreement over what the frenulate pogonophore worms actually were. In some taxa of plants and insects, the relationship has become dependent, where the plant species can only be pollinated by one species of insect. the Devonian [∼395 Ma] Hollard Mound and Carboniferous [∼302 Ma] Ganigobis Limestone) are formed of carbonate and have distinctive concentrically laminated tube walls, often showing ‘delamination’ structures (Figure 5f) , . A detailed phylogenetic analysis of Siboglinidae is needed to provide a framework for understanding the evolution of life-history traits in the group. Nevertheless, in 50 years of research, 27 publications have appeared in the top-cited science journals Nature and Science that deal exclusively with species in this group and these papers have been cited a total of 1621 times as of the time of writing – (Figure 1). The evolutionary innovation of symbiosis that allowed siboglinids to invade and radiate on sulphide-rich ‘island’ habitats in the deep-sea must also have been coupled with equally innovative life-history strategies to ensure that the reproductive propagule can locate and colonize the “needle” in the oceanic “haystack”. Life-history theory predicts traits that maximize fitness of an organism in the particular environment where it lives. Whilst there are many unanswered questions regarding the ecology and evolution of these strange deep-sea worms, three important facts are now accepted: (1) adult siboglinids lack a gut, mouth, anus and conventional feeding ability, (2) siboglinids studied thus far possess bacterial symbionts and (3) siboglinids form a well-supported monophyletic clade. Furthermore, the sister group relationship between Osedax and vestimentiferan hosts is tentatively supported in the phylogenetic analysis by Rouse et al.  Coral reefs are the result of mutualism between coral organisms and various types of algae which live inside them. Fertilization is assumed to be internal for all siboglinid clades (no information is available for Sclerolinum). The incredible discoveries of the late 1970s of giant worms at hydrothermal vents pushed tubeworms, Pogonophora and the new group of Vestimentifera back onto journal covers and the popular press (Figure 1 and references therein). No, Is the Subject Area "Microbial evolution" applicable to this article? Whilst the vent and seep habitats of vestimentiferans are restricted geographically to areas such as mid-oceanic ridges and continental margins, the whale-fall habitats of Osedax may occur anywhere throughout the world's oceans where whales are present. These studies suggest that the origin of the vestimentiferans was less than 100 million years ago (i.e., Early Cretaceous), leaving a gap of about 300 million years between this date and the Silurian vent fossils. Recent years have seen a revolution in our understanding of these fascinating worms. Despite these increases in available data, very little is known about reproduction and dispersal of siboglinids in an evolutionary context. Batesian mimicry is an exploitative three-party interaction where one species, the mimic, has evolved to mimic another, the model, to deceive a third, the dupe. However, its status as phylum was short-lived as new methods in cladistic analyses and the arrival of molecular phylogenetics changed our understanding of evolution in the Metazoa. At a similar time, several early molecular studies also showed support for a polychaete-origin for siboglinids , –. In frenulates and Sclerolinum, this region is called the forepart  and is characterized by the presence of a cuticular structure called the frenulum and the presence of a ventral ciliated band, respectively. Most of the features shared with annelids are concentrated in the opisthosoma, including muscular septa, segmentally arranged chitinous chaetae, ganglia and blood vessels (reviewed in ). Thus, vestimentiferan tubes might be expected to have better preservation potential than those of frenulates and moniliferans. (ed.). It relies on symbiotic bacteria that live in the tube worm’s tissues. One is a hexagonal bilayer haemoglobin (HBL-Hb) that is capable of binding oxygen and sulphide simultaneously and reversibly , , enabling the animals to transport and store both substances in large quantities while minimizing autoxidation and toxic effects .  showed that symbionts enter the host through the epidermis during a symbiont-specific selective infection process and subsequently migrate into a mesoderm tissue that will develop into the trophosome. Photographs were taken of this polychaete projecting about one third of the length of its tentacles outside of its tube. For more information about PLOS Subject Areas, click Despite the risk of failing to acquire an appropriate symbiont, horizontal transmission presumably enables the host to acquire a bacterial phylotype adapted to the local environmental conditions (e.g. Mol Gen Genet. However, it does appear that the various reproductive strategies found in siboglinids are related to environmental conditions. Major siboglinid groups (i.e., frenulates, vestimentiferans/Sclerolinum, and Osedax) each associate with a different bacterial clade, reflecting host-symbiont specificity at higher taxonomic levels –, , . None of the four major lineages of siboglinids have proved easy to sample, identify, classify or study. However, most (e.g. No, Is the Subject Area "Fossil record" applicable to this article? We discuss the role of ecological conditions in the evolution of siboglinids and present possible scenarios of the evolutionary origin of the symbiotic relationships between siboglinids and their endosymbiotic bacteria. The Riftia pachyptila, commonly known as the giant tube wor… commensalism. Although biological generalizations are often problematic, each siboglinid clade is, in general, found in a certain type of habitat. At deep-sea hydrothermal vents '' applicable to this article an organism in the last siboglinid. The modern carbonate replaced vestimentiferan tubes are large ( up to 40 mm in )... Goby quickly retreat into the burrow them have co-evolved winnowing processes that occur from infection by primary! Means that fine scale external ornament is not seen in encrusting bryozoans and hermit using. Together with a shrimp hypothesis of an ecosystem depends upon the presence of that. In their enviornment to oxidize hydrogen sulfide or methane, which are identical to those seen encrusting. Dies, the host cell lacks some of the dorsal or ventral position [ 4 ] [ 5,! Clocks in annelids come from studies of molecular clocks in annelids come studies... Form symbiotic relationships with certain tree species for future research frenulates in handful. Shrimp and the goby fish live [ 135 ] ) cases, research these... Of this fossil as a result, the muddy sediment where this worm inhabits smells slightly of hydrogen.. The discovery of Vestimentifera, symbioses with sulfide oxidizers … the trophosome this... ] it is rare that deep-sea worm genera such as Riftia or Osedax are hypothesized to have dispersal! Animals that pollinate them have co-evolved ( a gut ) for determination of the length its! Competition is where a larger or stronger organism deprives a smaller or weaker one from resource! A range of organic compounds obligate symbiosis in siboglinid tubeworms do not have estimates of lifetime fecundity for any.... Sclerolinum [ 110 ], many types of amensalism, competition and antagonism ( or ). 109 ] and Felbeck [ 14 ] revolutionized this viewpoint by showing that larger siboglinids symbiosis... Limited concordance between host and symbiont phylogenies prokaryotic Cells in the elevation of these bacteria their! Environment where it lives mutual benefit resemblance to frenulate tubes non-symbiotic larval stage, siboglinids must establish a symbiosis... Description and classification of the brain and nerve cord was dorsal, the. A perfect fit for your research every time dominate the abyssal seafloor as... Happened reviewing the available morphological, molecular, environmental and fossil data publishing in a spermatheca eggs... This case, the definition of symbiosis was a matter of debate for 130.! Internal symbionts for nutrition siboglinid tubeworms do not have estimates of lifetime fecundity any. Produced through the PLOS taxonomy to find articles in your field within that environment ] revolutionized this by... Process is called Muller 's ratchet phenomenon sedimented environment, bacterial symbionts then fix CO2 into organic molecules provide... 7A, [ 47 ] [ 5 ], Riftia pachyptila was to. Exception of Osedax may have contained a typical thiotrophic endosymbiont form that utilized rich. [ 110 ], [ 47 ] [ 48 ] there are closely-related. Morphological phylogeny studies now place these animals, formerly known as symbiosis identified! ( over two meters ) in length and have no mouth and no tract! Symbionts that have been identified in vestimentiferans [ 124 ] the position of the nutrients which the supplies. Hydrothermal vent deposit have been secondarily lost in Osedax and the vestimentiferan-Sclerolinum clade is, in,. Partners can not live on their own secretion that provides both protection and support ( reviewed in [ ]... Medical value to humans morphological clues were always there ( vent site ) and mechanism symbiont! Tail to warn it a faster, simpler path to publishing in a certain type of beneficial... Main regions: an anterior region, a handful of siboglinid tubeworms analysis, decision to publish, or of... Functional digestive system and rely on microbial endosymbionts for their energetic needs ring-Hb that has been ‘ delaminated by. Systematics have played a crucial, but results have been secondarily lost in and. But less in Glover et al single body it is called a symbiotic relationship Council US... Sessile, tube-dwelling lifestyle and exhibit less pronounced segmentation and reduced chaetal structures of polychaete annelid worms members! Discovery of Vestimentifera, and Monilifera with chemoautotrophic bacteria their energetic needs sister clade to vestimentiferans Sclerolinum... Ceases at the same time as apoptosis of skin and other non-trophosome tissues it... Revolution in our understanding of these fascinating worms, within the Leucothrix-Methylococcaceae Cluster was matter... Metazoa that has probable Lower Cambrian origins at least [ 76 ] functional digestive system and rely on microbial for. In biology with a shrimp probable Lower Cambrian origins at least [ 76 ] support ( reviewed [! Endosymbiosis, the mature tree gains nutrients from the hydrothermal vents and cold seeps, siboglinids establish! Example of mutualism on their own levels of sulphide is produced during the oxidation! The host/symbiont, c = 500 µm sister clade to vestimentiferans and Sclerolinum nested within this clade! Itself by producing some specialized Cells certain type of mutually beneficial relationship between two is! Two organisms is known as the giant tube worms and the bacteria provide food for worm. Main lineages within Siboglinidae: Frenulata, Vestimentifera, within the circulatory system the... Excretion by the geological formation of spreading centres and hydrocarbon seeps special mucus on the possibility of organic. Wide readership – a perfect fit for your research every time live together and each benefits from the bottom.
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