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

Abstract

The 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. 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. Key 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. In addition, 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.We also show how this worm, over the course of evolutionarymore » 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. These 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [1];  [4];  [4];  [4];  [4];  [1]
  1. Max Planck Inst. for Marine Microbiology, Bremen (Germany). Symbiosis Dept.
  2. Max Planck Inst. for Marine Microbiology, Bremen (Germany). Symbiosis Dept.; Univ. of Calgary, AB (Canada). Energy Bioenergineering and Geomicrobiology
  3. Max Planck Inst. for Marine Microbiology, Bremen (Germany). Symbiosis Dept.; HYDRA Inst. for Marine Sciences, Campo nell' Elba (Italy)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1336573
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 17; Journal Issue: 942; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English

Citation Formats

Wippler, Juliane, Kleiner, Manuel, Lott, Christian, Gruhl, Alexander, Abraham, Paul E., Giannone, Richard J., Young, Jacque C., Hettich, Robert L., and Dubilier, Nicole. Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis. United States: N. p., 2016. Web. doi:10.1186/s12864-016-3293-y.
Wippler, Juliane, Kleiner, Manuel, Lott, Christian, Gruhl, Alexander, Abraham, Paul E., Giannone, Richard J., Young, Jacque C., Hettich, Robert L., & Dubilier, Nicole. Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis. United States. doi:10.1186/s12864-016-3293-y.
Wippler, Juliane, Kleiner, Manuel, Lott, Christian, Gruhl, Alexander, Abraham, Paul E., Giannone, Richard J., Young, Jacque C., Hettich, Robert L., and Dubilier, Nicole. Mon . "Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis". United States. doi:10.1186/s12864-016-3293-y. https://www.osti.gov/servlets/purl/1336573.
@article{osti_1336573,
title = {Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis},
author = {Wippler, Juliane and Kleiner, Manuel and Lott, Christian and Gruhl, Alexander and Abraham, Paul E. and Giannone, Richard J. and Young, Jacque C. and Hettich, Robert L. and Dubilier, Nicole},
abstractNote = {The 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. 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. Key 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. In addition, 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.We also 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. These 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.},
doi = {10.1186/s12864-016-3293-y},
journal = {BMC Genomics},
issn = {1471-2164},
number = 942,
volume = 17,
place = {United States},
year = {2016},
month = {11}
}

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