AbstractChemosynthetic symbioses ar

Abstract
Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host's nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.

Symbioses between animals and chemosynthetic bacteria are widespread in Earth's oceans1. Animals from at least seven phyla have formed such symbioses, and even more chemosynthetic bacterial lineages have evolved symbioses with animal hosts1. Chemosynthetic symbionts can use a range of chemicals, such as sulfide, methane, hydrogen and carbon monoxide, to power their metabolism2,3,4. The hosts of chemosynthetic symbionts dominate some animal communities. For example, shallow-water lucinid bivalves, which host sulfur-oxidizing symbionts, often dominate the macrobenthic infaunal community in seagrass meadows, where they can reach densities greater than 3,500 individuals per square metre5,6. Their diversity in nature, their persistence over evolutionary timescales and their dominance in many habitats attest to the success of these symbiotic partnerships1.

Chemosynthetic symbionts are primarily considered ‘nutritional symbionts’, meaning their primary role is to provide nutrition for their hosts1,7. So far, most studies have focused on inorganic carbon fixation by the symbionts and the transfer of fixed organic carbon compounds to the hosts. In addition to organic carbon, all animals require a source of fixed nitrogen. However, nitrogen metabolism in chemosynthetic symbioses has received far less attention. Chemosynthetic symbionts have been shown to gain their nitrogen from ammonium or nitrate in their environment8,9,10 and co-occurring nitrogen-fixing and chemosynthetic symbionts have been found in cold-water corals11. Nitrogen fixation by chemosynthetic symbionts has long been hypothesized, but so far not yet shown12,13,14.

Our study focused mainly on the endosymbiosis between bivalves of the family Lucinidae and sulfur-oxidizing bacteria. Lucinids are by far the most diverse and widespread group of bivalves that host chemosynthetic symbionts15. There are at least 400 living species, occupying a range of habitats including mangrove sediments, seagrass beds, coral reef sediments and coastal mud and sand16. In seagrass habitats, lucinid bivalves and their sulfur-oxidizing symbionts are part of a nested symbiosis with seagrasses, which may be essential to the health and ecological success of seagrasses6. We focused on the symbiosis between Loripes lucinalis (Lamarck, 1818) and its endosymbionts. We also investigated a second symbiosis, that between stilbonematid nematodes and their sulfur-oxidizing ectosymbionts, because these symbionts are associated with the family Chromatiaceae, which contains a number of diazotrophic sulfur oxidizers17,18. Nematodes of the subfamily Stilbonematinae (family Desmodoridae) can be found worldwide in marine sulfidic habitats19. All known species have a dense coating of ectosymbionts on their cuticle, which are hypothesized to contribute to their host's nutrition19. The name Candidatus Thiosymbion oneisti will be proposed elsewhere for the nematode symbionts (Gruber-Vodicka et al., in preparation). We propose the name Candidatus Thiodiazotropha endoloripes for the symbiont of Loripes lucinalis, where ‘Thiodiazotropha’ refers to the sulfur-oxidizing (‘thio’) and nitrogen-fixing (‘diazotroph’) metabolism of the symbiont and ‘endoloripes’ (‘Endo-’, Greek from ἔνδον meaning ‘within’, ‘loripes’) refers to the endosymbiotic association with Loripes lucinalis, its bivalve host.

ผลลัพธ์ (อังกฤษ) 1:

AbstractChemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host's nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.Symbioses between animals and chemosynthetic bacteria are widespread in Earth's oceans1. Animals from at least seven phyla have formed such symbioses, and even more chemosynthetic bacterial lineages have evolved symbioses with animal hosts1. Chemosynthetic symbionts can use a range of chemicals, such as sulfide, methane, hydrogen and carbon monoxide, to power their metabolism2,3,4. The hosts of chemosynthetic symbionts dominate some animal communities. For example, shallow-water lucinid bivalves, which host sulfur-oxidizing symbionts, often dominate the macrobenthic infaunal community in seagrass meadows, where they can reach densities greater than 3,500 individuals per square metre5,6. Their diversity in nature, their persistence over evolutionary timescales and their dominance in many habitats attest to the success of these symbiotic partnerships1.Chemosynthetic symbionts are primarily considered 'nutritional symbionts', meaning their primary role is to provide nutrition for their hosts1,7. So far, most studies have focused on inorganic carbon fixation by the symbionts and the transfer of fixed organic carbon compounds to the hosts. In addition to organic carbon, all animals require a source of fixed nitrogen. However, nitrogen metabolism in chemosynthetic symbioses has received far less attention. Chemosynthetic symbionts have been shown to gain their nitrogen from ammonium or nitrate in their environment8,9,10 and co-occurring nitrogen-fixing and chemosynthetic symbionts have been found in cold-water corals11. Nitrogen fixation by chemosynthetic symbionts has long been hypothesized, but so far not yet shown12,13,14.Our study focused mainly on the endosymbiosis between bivalves of the family Lucinidae and sulfur-oxidizing bacteria. Lucinids are by far the most diverse and widespread group of bivalves that host chemosynthetic symbionts15. There are at least 400 living species, occupying a range of habitats including mangrove sediments, seagrass beds, coral reef sediments and coastal mud and sand16. In seagrass habitats, lucinid bivalves and their sulfur-oxidizing symbionts are part of a nested symbiosis with seagrasses, which may be essential to the health and ecological success of seagrasses6. We focused on the symbiosis between Loripes lucinalis (Lamarck, 1818) and its endosymbionts. We also investigated a second symbiosis, that between stilbonematid nematodes and their sulfur-oxidizing ectosymbionts, because these symbionts are associated with the family Chromatiaceae, which contains a number of diazotrophic sulfur oxidizers17,18. Nematodes of the subfamily Stilbonematinae (family Desmodoridae) can be found worldwide in marine sulfidic habitats19. All known species have a dense coating of ectosymbionts on their cuticle, which are hypothesized to contribute to their host's nutrition19. The name Candidatus Thiosymbion oneisti will be proposed elsewhere for the nematode symbionts (Gruber-Vodicka et al., in preparation). We propose the name Candidatus Thiodiazotropha endoloripes for the symbiont of Loripes lucinalis, where ' Thiodiazotropha ' refers to the sulfur-oxidizing (thio) and nitrogen-fixing (' diazotroph ') of the symbiont metabolism and ' endoloripes ' (' Endo-', from Greek endon ' within', ' meaning loripes ') refers to the endosymbiotic association with Loripes lucinalis, its host bivalve.