Bathymodiolus mussels live in symbiosis with intracellular sulfur-oxidizing (SOX) bacteria that provide them with nutrition. We sequenced the SOX symbiont genomes from two Bathymodiolus species.
Comparison of these symbiont genomes with those of their closest relatives revealed that the symbionts have undergone genome rearrangements, and up to 35% of their genes may have been acquired by horizontal gene transfer. Many of the genes specific to the symbionts were homologs of virulence genes. We discovered an abundant and diverse array of genes similar to insecticidal toxins of nematode and aphid symbionts, and toxins of pathogens such as Yersinia and Vibrio. Transcriptomics and proteomics revealed that the SOX symbionts express the toxin-related genes (TRGs) in their hosts.
We hypothesize that the symbionts use these TRGs in beneficial interactions with their host, including protection against parasites. This would explain why a mutualistic symbiont would contain such a remarkable ‘arsenal’ of TRGs.
ELife digest. Although bacteria are commonly associated with causing illness, many are actually beneficial to the organism they live in or on. The phenomenon of one species helping another to survive is known as symbiosis.Animals thrive at hydrothermal vents in the deep sea because of their partnerships with symbiotic bacteria. The bacteria use the geochemical energy found at hydrothermal vents to convert carbon into sugars, thus providing their animal hosts with essential nutrients. Unlike the symbiotic communities that associate with humans and other mammals, in which thousands of bacterial species co-exist, deep-sea mussels associate with just one or two species of symbiotic bacteria. This relative simplicity is ideal for investigating how the intimate associations between animals and bacteria work.Genes contain the instructions cells and organisms need to survive, and so one way that researchers investigate symbiosis is by studying the genes of the organisms involved. Such studies of beneficial bacteria are beginning to reveal that the molecular mechanisms involved in symbiosis are remarkably similar to those responsible for the harmful effects produced by some bacteria.By performing genetic sequencing on the symbiotic bacteria from deep-sea mussels, Sayavedra et al.
Have discovered that the bacteria have an unusually large number of toxin-like genes, and that all of these genes are active in the bacteria when they are inside host mussels. This was unexpected, as the bacteria are known to benefit their mussel hosts. The toxin-like genes from the symbiotic bacteria are similar to toxins found in the bacteria that cause diseases such as cholera and the plague in humans and other animals.Sayavedra et al. Suggest that the symbiotic bacteria have ‘tamed’ these toxins to use them in beneficial interactions with their host. For example, some of the toxins could help the bacteria and mussels to recognize and interact with each other, and others could help to protect the mussel host from its natural enemies. The next step will be to test these ideas, which will be challenging as the mussels cannot be bred in the laboratory. Mussels of the genus Bathymodiolus dominate deep-sea hydrothermal vents and cold seeps worldwide.
The key to their ecological and evolutionary success is their symbiosis with chemosynthetic bacteria that provide them with nutrition (; ). Bathymodiolus mussels host their symbionts inside specialized gill epithelial cells called bacteriocytes (; ).Their filtering activity exposes Bathymodiolus mussels to a plethora of diverse microbes in their environment.
Despite this, they are colonized by only one or a few specific types of chemosynthetic symbionts. Some mussel species associate exclusively with sulfur-oxidizing (SOX) symbionts that use reduced sulfur compounds and sometimes hydrogen as an energy source, and carbon dioxide as a carbon source. Some have only methane-oxidizing (MOX) symbionts that use methane as an energy source and carbon source.
Some mussel species host both types in a dual symbiosis (;;;; ). In all species except one, a single 16S rRNA phylotype for each type of symbiont (SOX or MOX) is found in the gills.
There are more than 30 described Bathymodiolus species, and most associate with a characteristic symbiont phylotype, which is not found in other species.Although these associations are clearly very specific, the molecular mechanisms that underpin this specificity are still unknown. No chemosynthetic symbiont has ever been obtained in pure culture. Therefore, molecular methods for investigating uncultured microbes have been essential for understanding their biodiversity, function, and evolution (reviewed by ).The Bathymodiolus symbionts are assumed to be horizontally transmitted, which means that each new host generation must take up their symbionts from the surrounding environment or co-occurring adults (;;;; ). To initiate the symbiosis, hosts and symbionts must have evolved highly specific recognition and attachment mechanisms. Once they have been recognized, the symbionts need to enter host cells and avoid immediate digestion, just like other intracellular symbionts such as Burkholderia rhizoxinica and Rhizobium leguminosarum, or pathogens such as Legionella, Listeria, or Yersinia (; ). Indeed, like many intracellular pathogens, the Bathymodiolus symbionts seem to induce a loss of microvilli on the cells they colonize (;;; ). Finally, the symbionts achieve dense populations inside the host cells (e.g.,; ).
Therefore, they must be able to avoid immediate digestion by their hosts. Although the mechanisms of host cell entry and immune evasion have been extensively studied in pathogens and plant–microbe associations such as the rhizobia-legume symbiosis, far less is known about the mechanisms beneficial symbionts use to enter and survive within animal host cells.The symbiosis between Vibrio fisheri bacteria and Euprymna scolopes squid is one of the few beneficial host-microbe associations where the molecular mechanisms of host-symbiont interaction have been investigated. A number of factors are involved in initiating this symbiosis such as the symbiont-encoded ‘TCT toxin’, which is related to the tracheal cytotoxin of Bordetella pertussis. A few studies of intracellular insect symbionts have shown that they use type III and type IV secretion systems to establish and maintain their association with their host (reviewed by; ).
These secretion systems are commonly used by intracellular pathogens to hijack host cell processes, allowing their entry and survival within host cells (e.g.,;; ). An example is the Sodalis symbionts of aphids and weevils, which use a type III secretion system for entry to the host cell and are thought to have evolved from pathogens (; ). The virulence determinants of their pathogenic ancestors might therefore have been co-opted for use in beneficial interactions with their insect hosts.In contrast to the Sodalis symbionts of insects and the Vibrio symbionts of squid, the Bathymodiolus SOX symbionts are not closely related to any known pathogens. Moreover, because they fall interspersed between free-living SOX bacteria in 16S rRNA phylogenies, they are hypothesized to have evolved multiple times from free-living ancestors.
Comparative genomics is a powerful tool for identifying the genomic basis of beneficial and pathogenic interactions, particularly if the symbionts or pathogens have close free-living relatives that do not associate with a host (e.g.,;; ). Genomes of closely related free-living and symbiotic relatives of Bathymodiolus SOX symbionts were recently published. Their closest free-living relatives are marine SOX bacteria called SUP05, which are abundant in the world's oceans, particularly in oxygen minimum zones (OMZs) and hydrothermal plumes (;;;;; ). The Bathymodiolus SOX symbionts and SUP05 bacteria form a monophyletic clade together with the SOX symbionts of vesicomyid clams based on 16S rRNA gene phylogenies (; ). Closed genomes are available for the symbionts of two clam species (; ).All members of this monophyletic group (the mussel and clam symbionts, and SUP05) share similar core metabolic features. They are all capable of autotrophic growth, and all use reduced sulfur compounds as an energy source (; ).
They can differ in auxiliary metabolic capabilities such as hydrogen oxidation, nitrate reduction, or mixotrophy (;;; ). However, the major difference between these organisms is their lifestyle: SUP05 bacteria are exclusively free-living. The clam symbionts are exclusively host-associated, are vertically transmitted, and have reduced genomes. The Bathymodiolus symbionts appear to have adapted to both niches, as they have a host-associated stage and are assumed to also have a free-living stage.The goal of this study was to identify the genomic basis of host-symbiont interactions in Bathymodiolus symbioses.
We used high-throughput sequencing and binning techniques to assemble the first essentially complete draft genomes of the SOX symbionts from Bathymodiolus mussels. We used comparative genomics of the symbionts' genomes to those of their close free-living and obligate symbiotic relatives to reveal genes potentially involved in Bathymodiolus host-symbiont interactions. We used phylogenetics and bioinformatic prediction of horizontally acquired genes to investigate the origins of these genes. Finally, we used transcriptomics and proteomics to determine whether potential host-symbiont interaction genes are being expressed by the symbionts in their host.
We sequenced the genomes of the SOX symbionts from three Bathymodiolus individuals: two were Bathymodiolus azoricus from the Menez Gwen vent field on the northern Mid-Atlantic Ridge (MAR). We refer to these as BazSymA and BazSymB. The third mussel individual was an undescribed Bathymodiolus species (BspSym), from the Lilliput hydrothermal vent on the southern MAR (SMAR). Symbiont draft genomes from each individual were almost complete (see ‘Materials and methods’). Despite different sequencing and assembly strategies, the draft genomes were 90.7–97.7% complete. The total assembly sizes were between 1.7 and 2.3 Mbp, on 52 to 506 contigs.
Each draft genome contained one copy of the 16S rRNA gene. The BazSymB assembly only contained an 829 bp fragment of the 16S rRNA gene; however, we PCR amplified and sequenced this gene from the DNA used to generate the metagenome. The 16S rRNA genes from the two B. Azoricus symbionts were 100% identical and were 99.3% identical to BspSym. The core metabolic potential of the Bathymodiolus SOX symbionts is described in -Symbiont metabolism. A detailed description of the genomes is beyond the scope of this article and will be published elsewhere.
Ex - Integrantes.Keith Levene (Guitarras, Teclados e Diversos, 1978-1983)JahWobble (Baixo, 1978-1980)Jim Walker (Bateria, 1978)Vivian Jackson(Bateria, 1979)David Humphrey (Bateria, fevereiro de 1979)RichardDudanski (Bateria, abril - setembro de 1979)Karl Burns (Bateria, setembro de1979)Martin Atkins (Bateria e Diversos, 1979-1980, 1982-1985)Steve New(Guitarra, 1980, R.I.P 2010)Ken Lockie (Teclados, 1982)Pete Jones(Baixo, 1982-1983)John Mcgeoch (Guitarra, 1986-1992, R.I.P 2004)AllanDias (Baixo, 1986-1992). A. B.
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