Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis

BMC Genomics

Research Article

Robert L. Hettich¹  Richard J. Giannone¹  Paul E. Abraham¹  Jacque C. Young²  Alexander Gruhl³  Nicole Dubilier³  Manuel Kleiner⁴  Christian Lott⁵  Juliane Wippler⁶ 

[1] Oak Ridge National Laboratory, Chemical Sciences Division, Oak Ridge, Tennessee, 1 Bethel Valley Rd, 37831, Oak Ridge, TN, USA;Oak Ridge National Laboratory, Chemical Sciences Division, Oak Ridge, Tennessee, 1 Bethel Valley Rd, 37831, Oak Ridge, TN, USA;Present Address: Saul Ewing LLP, 1500 Market Street, 37th Floor, 19102-2186, Philadelphia, PA, USA;Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany;Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany;Energy Bioengineering and Geomicrobiology Research Group, University of Calgary, T2N 1N4, Calgary, AB, Canada;Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany;HYDRA Institute for Marine Sciences, Elba Field Station, Via del Forno 80, 57034, Campo nell’ Elba, (LI), Italy;Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany;Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany;

关键词: RNA-Seq;    Annelida;    Oligochaeta;    Phallodrilinae;    PGRP;    FREP;    SRCR;    Respiratory pigment;    Carbon monoxide;    Immunology;    Chemosynthetic symbiosis;   

DOI  :  10.1186/s12864-016-3293-y

 received in 2016-06-04, accepted in 2016-11-15,  发布年份 2016

来源: Springer

【 摘 要 】

BackgroundThe gutless marine worm Olavius algarvensis has a completely reduced digestive and excretory system, and lives in an obligate nutritional symbiosis with bacterial symbionts. While considerable knowledge has been gained of the symbionts, the host has remained largely unstudied. Here, we generated transcriptomes and proteomes of O. algarvensis to better understand how this annelid worm gains nutrition from its symbionts, how it adapted physiologically to a symbiotic lifestyle, and how its innate immune system recognizes and responds to its symbiotic microbiota.ResultsKey adaptations to the symbiosis include (i) the expression of gut-specific digestive enzymes despite the absence of a gut, most likely for the digestion of symbionts in the host's epidermal cells; (ii) a modified hemoglobin that may bind hydrogen sulfide produced by two of the worm’s symbionts; and (iii) the expression of a very abundant protein for oxygen storage, hemerythrin, that could provide oxygen to the symbionts and the host under anoxic conditions. Additionally, we identified a large repertoire of proteins involved in interactions between the worm's innate immune system and its symbiotic microbiota, such as peptidoglycan recognition proteins, lectins, fibrinogen-related proteins, Toll and scavenger receptors, and antimicrobial proteins.ConclusionsWe show how this worm, over the course of evolutionary time, has modified widely-used proteins and changed their expression patterns in adaptation to its symbiotic lifestyle and describe expressed components of the innate immune system in a marine oligochaete. Our results provide further support for the recent realization that animals have evolved within the context of their associations with microbes and that their adaptive responses to symbiotic microbiota have led to biological innovations.

【 授权许可】

CC BY   
© The Author(s). 2016