RESUMEN
Gutless phallodrilines are marine annelid worms without a mouth or gut, which live in an obligate association with multiple bacterial endosymbionts that supply them with nutrition. In this study, we discovered an unusual symbiont community in the gutless phallodriline Inanidrilus exumae that differs markedly from the microbiomes of all 22 of the other host species examined. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization revealed that I. exumae harbors cooccurring gamma-, alpha-, and deltaproteobacterial symbionts, while all other known host species harbor gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic sulfur oxidizer "Candidatus Thiosymbion" that occurs in all other gutless phallodriline hosts does not appear to be present in I. exumae Instead, I. exumae harbors a bacterial endosymbiont that resembles "Ca Thiosymbion" morphologically and metabolically but originates from a novel lineage within the class Gammaproteobacteria This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA gene sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from that of "Ca Thiosymbion." Sulfur globules in the Gamma 4 symbiont cells, as well as the presence of genes characteristic for autotrophy (cbbL) and sulfur oxidation (aprA), indicate that this symbiont is a chemoautotrophic sulfur oxidizer. Our results suggest that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae and appears to have displaced the "Ca Thiosymbion" symbionts originally associated with these hosts.IMPORTANCE All 22 gutless marine phallodriline species examined to date live in a highly specific association with endosymbiotic, chemoautotrophic sulfur oxidizers called "Ca Thiosymbion." These symbionts evolved from a single common ancestor and represent the ancestral trait for this host group. They are transmitted vertically and assumed to be in transition to becoming obligate endosymbionts. It is therefore surprising that despite this ancient, evolutionary relationship between phallodriline hosts and "Ca Thiosymbion," these symbionts are apparently no longer present in Inanidrilus exumae They appear to have been displaced by a novel lineage of sulfur-oxidizing bacteria only very distantly related to "Ca Thiosymbion." Thus, this study highlights the remarkable plasticity of both animals and bacteria in establishing beneficial associations: the phallodriline hosts were able to acquire and maintain symbionts from two very different lineages of bacteria, while sulfur-oxidizing bacteria from two very distantly related lineages were able to independently establish symbiotic relationships with phallodriline hosts.
Asunto(s)
Chromatiaceae/fisiología , Oligoquetos/microbiología , Simbiosis , Animales , Chromatiaceae/clasificación , Chromatiaceae/genética , Genes Bacterianos , Hibridación Fluorescente in Situ , Filogenia , ARN Bacteriano/análisis , ARN Ribosómico 16S/análisis , Análisis de Secuencia de ARNRESUMEN
The male genital duct in Tubificidae consists of a funnel, a vas deferens, an atrium, and, frequently, a copulatory structure. There may also be a diffuse or compact prostate gland in association with the duct. The morphogenesis of this duct is described for Rhyacodrilus coccineus and Monopylephorus rubroniveus (Rhyacodrilinae). The funnel and vas deferens in both species originate from peritoneal (mesodermal) cells in the posterior septum in the testis segment. The atrium in R. coccineus develops from a primary epidermal (ectodermal) invagination. A typical atrium is not formed in M. rubroniveus; the entire duct is of mesodermal origin. In the latter species, a shallow epidermal invagination occurs, into which both male ducts open, but it bears resemblance to a copulatory structure, which usually forms from a secondary invagination, rather than to a proper atrium. We therefore conclude that M. rubroniveus lacks an atrium. The copulatory structure is termed the male bursa. Both species have diffuse prostate glands that differentiate from peritoneal (mesodermal) cells surrounding the male duct. In R. coccineus the cells cover the atrium, whereas in M. rubroniveus they cover only a part of the vas deferens. The development of the spermathecae and female ducts is also examined. The spermatheca is of ectodermal origin in both studied species, i.e., it forms as an invagination of the epidermis. The female duct develops from peritoneal (mesodermal) cells in the posterior septum of the ovary segment. However, in M. rubroniveus the first sign of the duct disappears and a proper duct never develops.
Asunto(s)
Oligoquetos/crecimiento & desarrollo , Animales , Femenino , Genitales Femeninos/crecimiento & desarrollo , Genitales Masculinos/crecimiento & desarrollo , Masculino , Conducto Deferente/crecimiento & desarrolloRESUMEN
The life cycle of the histozoic myxozoan parasite Henneguya nuesslini was investigated in two salmonid host species. Naive brown trout, Salmo trutta, and brook trout, Salvelinus fontinalis, were experimentally infected in two trials by triactinomyxon type actinospores from naturally infected Tubifex tubifex. In exposed common carp, Cyprinus carpio, no myxospore production was detected. The parasite formed cysts with mature myxospores in the connective tissue of the fish 102 days post-exposure. The morphology of both actinosporean and myxosporean stages was described by light microscopy and a 1417-bp fragment of the 18S rDNA gene was sequenced. Sequence analysis confirmed the absolute congruence of the two developmental stages and assisted in determining species identity. Host range, tissue specificity and myxospore measurements provided sufficiently distinctive features to confirm species validity and were thus crucial for identification. The triactinomyxon spores had 16 secondary germ cells, unique dimensions, a very opaque sporoplasm matrix and three conspicuously protruding, pyriform polar capsules. This is the first record of a Henneguya sp. life cycle with a triactinomyxon-type actinospore, which suggests a close relationship with the Myxobolus group and a polyphyletic origin of the genus Henneguya.
Asunto(s)
Eucariontes/fisiología , Esporas Protozoarias/citología , Trucha/parasitología , Animales , Secuencia de Bases , Pesos y Medidas Corporales , Cartilla de ADN , Eucariontes/citología , Eucariontes/genética , Datos de Secuencia Molecular , Oligoquetos/parasitología , ARN Ribosómico 18S/genética , Análisis de Secuencia de ADNRESUMEN
Tubificids are aquatic clitellate worms, but recent analyses of morphological characters suggested that this family, as currently recognized, is paraphyletic. Sequences of the 18S rDNA gene of 40 protostome worm species (including 13 representatives of the Tubificidae) and 2 mollusc species were cladistically analyzed to test the monophyly of the Tubificidae and that of some of its constituent subfamilies. Under all alignments tested, the same general phylogenetic pattern emerged. The data support the idea that the Naididae, another clitellate taxon, is associated with some "rhyacodriline" groups within the Tubificidae. The data also corroborate the idea that the Tubificinae and the Limnodriloidinae are monophyletic but indicate that the Rhyacodrilinae and the Phallodrilinae are not. Bathydrilus does not appear to be closely related to other "phallodriline" genera.
Asunto(s)
ADN Ribosómico/genética , Oligoquetos/clasificación , Oligoquetos/genética , ARN Ribosómico 18S/genética , Animales , Bases de Datos Factuales , Filogenia , Poliquetos/clasificación , Poliquetos/genéticaRESUMEN
Four species of actinosporeans are described from marine oligochaetes (all Tubificidae) from the Great Barrier Reef, Queensland, Australia. They developed in the coelom of the oligochaete and produced spores in groups of eight in the pansporocysts. The new genus Endocapsa is proposed within the family Sphaeractinomyxidae Janiszewska, 1957 on the basis that mature spores have small valve cell processes and non-protruding polar capsules. The type-species, Endocapsa rosulata n. sp., has three valve cell processes, which resemble a rosette, and submerged polar capsules. It infected Heterodrilus cf. keenani from Heron Island and morphologically similar parasites occurred in Thalassodrilides cf. gurwitschi and Heronidrilus sp. from Lizard Island. E. stepheni n. sp. has asymmetrical valve cell processes and submerged polar capsules. It was found in H. cf. keenani and H. queenslandicus from Heron Island. Sphaeractinomyxon leptocapsula n. sp. has thin widely spaced polar capsules and is described from Heronidrilus sp. from Lizard Island. S. ersei Hallett, O'Donoghue & Lester, 1998 infected Tubificidae gen. sp. from Heron Island and S. cf. ersei occurred in Bathydrilus sp., Thalassodrilides cf. gurwitschi and Limnodriloides lateroporus from Lizard Island.
Asunto(s)
Eucariontes/clasificación , Oligoquetos/parasitología , Animales , Eucariontes/crecimiento & desarrollo , Queensland , Agua de MarRESUMEN
To investigate the phylogenetic relationships of leeches, branchiobdellidans, and acanthobdellidans, whole nuclear 18S rDNA and over 650 bp of mitochondrial cytochrome c oxidase subunit I were acquired from 101 annelids, including 36 leeches, 18 branchiobdellidans, Acanthobdella peledina, as well as 28 oligochaetes and combined with homologous data for 17 polychaete outgroup taxa. Parsimony analysis of the combined aligned dataset supported monophyly of leeches, branchiobdellidans, and acanthobdellidans in 100% of jackknife replicates. Monophyly of the oligochaete order Lumbriculida with Acanthobdellida, Branchiobdellida, and Hirudinea was supported in 84% of jackknife replicates. These results provide support for the hypotheses that leeches and branchiobdellidans are sister groups, that acanthobdellidans are sister to them, and that together with the family Lumbriculidae they all constitute a clade within Oligochaeta. Results support synonymy of the classes Clitellata and the more commonly used Oligochaeta. Leeches branchiobdellidans, and acanthobdellidans should be regarded as orders equal to their closest relatives, the order Lumbriculida.
Asunto(s)
Sanguijuelas/clasificación , Filogenia , Animales , ADN Ribosómico/genética , Sanguijuelas/genética , ARN Ribosómico 18S/genética , Especificidad de la EspecieRESUMEN
Stable associations of more than one species of symbiont within a single host cell or tissue are assumed to be rare in metazoans because competition for space and resources between symbionts can be detrimental to the host. In animals with multiple endosymbionts, such as mussels from deep-sea hydrothermal vents and reef-building corals, the costs of competition between the symbionts are outweighed by the ecological and physiological flexibility gained by the hosts. A further option for the coexistence of multiple symbionts within a host is if these benefit directly from one another, but such symbioses have not been previously described. Here we show that in the gutless marine oligochaete Olavius algarvensis, endosymbiotic sulphate-reducing bacteria produce sulphide that can serve as an energy source for sulphide-oxidizing symbionts of the host. Thus, these symbionts do not compete for resources but rather share a mutalistic relationship with each other in an endosymbiotic sulphur cycle, in addition to their symbiotic relationship with the oligochaete host.