Abstract
The relationships between hydrothermal vent tubeworms and sulfide-oxidizing bacteria have served as model associations for understanding chemoautotrophy and endosymbiosis. Numerous studies have focused on the physiological and biochemical adaptations that enable these symbioses to sustain some of the highest recorded carbon fixation rates ever measured. However, far fewer studies have explored the molecular mechanisms underlying the regulation of host and symbiont interactions, specifically those mediated by the innate immune system of the host. To that end, we conducted a series of studies where we maintained the tubeworm, Ridgeia piscesae, in high-pressure aquaria and examined global and quantitative changes in gene expression via high-throughput transcriptomics and quantitative real-time PCR (qPCR). We analyzed over 32,000 full-length expressed sequence tags as well as 26 Mb of transcript sequences from the trophosome (the organ that houses the endosymbiotic bacteria) and the plume (the gas exchange organ in contact with the free-living microbial community). R. piscesae maintained under conditions that promote chemoautotrophy expressed a number of putative cell signaling and innate immunity genes, including pattern recognition receptors (PRRs), often associated with recognizing microbe-associated molecular patterns (MAMPs). Eighteen genes involved with innate immunity, cell signaling, cell stress and metabolite exchange were further analyzed using qPCR. PRRs, including five peptidoglycan recognition proteins and a Toll-like receptor, were expressed significantly higher in the trophosome compared to the plume. Although PRRs are often associated with mediating host responses to infection by pathogens, the differences in expression between the plume and trophosome also implicate similar mechanisms of microbial recognition in interactions between the host and symbiont. We posit that regulation of this association involves a molecular “dialogue” between the partners that includes interactions between the host’s innate immune system and the symbiont.
Highlights
Deep-sea hydrothermal vents host highly productive ecosystems based on microbial chemoautotrophy
We identified pattern recognition receptors (PRRs) involved with recognition of microbe-associated molecular patterns (MAMPs), including peptidoglycan recognition proteins, PGRPs, [58] a Toll-like receptor, TLR [59,60] and a lipoprotein receptor [61]
When considered in the context of previous research on the structural morphology within the trophosomes of siboglinid tubeworms [12,34,35,36,37,47,62], the data presented support the hypothesis that an orderly but complex host and symbiont cell cycle is important in maintaining symbiostasis. These results demonstrate differential expression of innate immunity genes between the trophosome and the plume, suggesting that different strategies are adopted by the Category MAMP recognition
Summary
Deep-sea hydrothermal vents host highly productive ecosystems based on microbial chemoautotrophy (for review see [1,2]) Many of these vent communities are dominated by siboglinid annelid tubeworms that are mouthless and gutless, and symbiotic with sulfide-oxidizing, chemoautotrophic bacteria. The symbionts fix inorganic carbon using energy derived from oxidizing sulfide [5] using oxygen or nitrate [6,7,8] They receive all metabolites necessary for chemoautotrophy from the host, which acquires the majority of these substrates through the branchial plume, the respiratory organ that extends outside the host’s chitinous tube directly into vent fluid-enriched seawater. The symbionts of an adult worm are never in contact with the external milieu, even though the bacteria are likely environmentally transmitted with each host generation [11]
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