Energy metabolic relationship of Lamellibrachia satsuma with its endosymbiont revealed by metagenomic analysis

Abstract

Lamellibrachia satsuma is a vestimentiferan tube worm lack mouth, gut and anus. They are nourished by chemoautotrophic bacterial endosymbionts growing in a specialized tissue called the trophosome. The L. satsuma was found at depth 82-110 m in Kagosima Bay, the shallowest depth record for a vestimentiferan. In this study, a sample of trophosome contents from the tubeworm was sequenced by Illumina HiSeq 2000. Data were assembled using SOAP de novo. Assembled data were submitted to the IMG/MER pipeline. Metagenomic analysis suggests that they harbor mostly γ-proteobacterial endosymbiont in the trophosome very closely related to the endosymbiont of the vent tubeworm Riftia pachyptila. The genes involved in carbon and sulfur metabolism indicate a sulfide-oxidizing chemoautotrophic endosymbiont. The symbionts contain all genes required for sulfur-oxidizing metabolism including those needed for the oxidation of reduced sulfur compounds mediated through the cytoplasmic enzymes adenylylsulfate reductase (AprA/AprB), periplasmic sulfite oxidase enzyme complex (Sox). The membrane bound respiratory nitrate reductase (NarI), a cytochrome cd1/ nitrite reductase (Nir), nitric oxide reductase (Nor) and nitric-oxide reductase (Nos) genes required for nitrate assimilation are also found in these symbionts. Surprisingly, the endosymbiont harbors genes for two different carbon fixation pathways, the Calvin-Benson-Bassham (CBB) cycle as well as the reductive tricarboxylic acid (rTCA) cycle, as has been reported in the endosymbiont of the various tubeworms like Riftia pachyptila, Tevnia jerichonana, Escarpia laminata and Lamellibrachia spp. This study suggests that, regardless of different geographical location, most of the vestimentiferan tubeworms might possess endosymbiont of common energy metabolism capability.