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Title: Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches

Abstract

By combining genomics and isotope imaging analysis using high-resolution secondary ion mass spectrometry (NanoSIMS), we examined the function and evolution of Bacteroidales ectosymbionts of the protistBarbulanymphafrom the hindguts of the wood-eating cockroachCryptocercus punctulatus. In particular, we investigated the structure of ectosymbiont genomes, which, in contrast to those of endosymbionts, has been little studied to date, and tested the hypothesis that these ectosymbionts fix nitrogen. Unlike with most obligate endosymbionts, genome reduction has not played a major role in the evolution of the Barbulanympha ectosymbionts. Instead, interaction with the external environment has remained important for this symbiont as genes for synthesis of transporters, outer membrane proteins, lipopolysaccharides, and lipoproteins have been retained. The ectosymbiont genome carried two complete operons for nitrogen fixation, a urea transporter, and a urease, indicating the availability of nitrogen as a driving force behind the symbiosis. NanoSIMS analysis ofC. punctulatushindgut symbionts exposedin vivoto15N2 supports the hypothesis thatBarbulanymphaectosymbionts are capable of nitrogen fixation. This genomic andin vivofunctional investigation of protist ectosymbionts highlights the diversity of evolutionary forces and trajectories that shape symbiotic interactions. The ecological and evolutionary importance of symbioses is increasingly clear, but the overall diversity of symbiotic interactions remains poorly explored. Here in this study, wemore » investigated the evolution and nitrogen fixation capabilities of ectosymbionts attached to the protist Barbulanympha from the hindgut of the wood-eating cockroach Cryptocercus punctulatus. In addressing genome evolution of protist ectosymbionts, our data suggest that the ecological pressures influencing the evolution of extracellular symbionts clearly differ from intracellular symbionts and organelles. Using NanoSIMS analysis, we also obtained direct imaging evidence of a specific hindgut microbe playing a role in nitrogen fixation. These results demonstrate the power of combining NanoSIMS and genomics tools for investigating the biology of uncultivable microbes. This investigation paves the way for a more precise understanding of microbial interactions in the hindguts of wood-eating insects and further exploration of the diversity and ecological significance of symbiosis between microbes.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [1]
  1. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Botany; Canadian Inst. for Advanced Research, Toronto, ON (Canada)
  2. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  3. North Carolina State Univ., Raleigh, NC (United States). Dept. of Entomology
  4. Univ. of Victoria, BC (Canada). Dept. of Biology
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE; Canadian Institute for Advanced Research (CIFAR)
OSTI Identifier:
1341997
Report Number(s):
LLNL-JRNL-672456
Journal ID: ISSN 0099-2240
Grant/Contract Number:  
AC52-07NA27344; 227301; 011-LW-039; SCW1039
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 82; Journal Issue: 15; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS

Citation Formats

Tai, Vera, Carpenter, Kevin J., Weber, Peter K., Nalepa, Christine A., Perlman, Steve J., and Keeling, Patrick J. Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches. United States: N. p., 2016. Web. https://doi.org/10.1128/AEM.00611-16.
Tai, Vera, Carpenter, Kevin J., Weber, Peter K., Nalepa, Christine A., Perlman, Steve J., & Keeling, Patrick J. Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches. United States. https://doi.org/10.1128/AEM.00611-16
Tai, Vera, Carpenter, Kevin J., Weber, Peter K., Nalepa, Christine A., Perlman, Steve J., and Keeling, Patrick J. Fri . "Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches". United States. https://doi.org/10.1128/AEM.00611-16. https://www.osti.gov/servlets/purl/1341997.
@article{osti_1341997,
title = {Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches},
author = {Tai, Vera and Carpenter, Kevin J. and Weber, Peter K. and Nalepa, Christine A. and Perlman, Steve J. and Keeling, Patrick J.},
abstractNote = {By combining genomics and isotope imaging analysis using high-resolution secondary ion mass spectrometry (NanoSIMS), we examined the function and evolution of Bacteroidales ectosymbionts of the protistBarbulanymphafrom the hindguts of the wood-eating cockroachCryptocercus punctulatus. In particular, we investigated the structure of ectosymbiont genomes, which, in contrast to those of endosymbionts, has been little studied to date, and tested the hypothesis that these ectosymbionts fix nitrogen. Unlike with most obligate endosymbionts, genome reduction has not played a major role in the evolution of the Barbulanympha ectosymbionts. Instead, interaction with the external environment has remained important for this symbiont as genes for synthesis of transporters, outer membrane proteins, lipopolysaccharides, and lipoproteins have been retained. The ectosymbiont genome carried two complete operons for nitrogen fixation, a urea transporter, and a urease, indicating the availability of nitrogen as a driving force behind the symbiosis. NanoSIMS analysis ofC. punctulatushindgut symbionts exposedin vivoto15N2 supports the hypothesis thatBarbulanymphaectosymbionts are capable of nitrogen fixation. This genomic andin vivofunctional investigation of protist ectosymbionts highlights the diversity of evolutionary forces and trajectories that shape symbiotic interactions. The ecological and evolutionary importance of symbioses is increasingly clear, but the overall diversity of symbiotic interactions remains poorly explored. Here in this study, we investigated the evolution and nitrogen fixation capabilities of ectosymbionts attached to the protist Barbulanympha from the hindgut of the wood-eating cockroach Cryptocercus punctulatus. In addressing genome evolution of protist ectosymbionts, our data suggest that the ecological pressures influencing the evolution of extracellular symbionts clearly differ from intracellular symbionts and organelles. Using NanoSIMS analysis, we also obtained direct imaging evidence of a specific hindgut microbe playing a role in nitrogen fixation. These results demonstrate the power of combining NanoSIMS and genomics tools for investigating the biology of uncultivable microbes. This investigation paves the way for a more precise understanding of microbial interactions in the hindguts of wood-eating insects and further exploration of the diversity and ecological significance of symbiosis between microbes.},
doi = {10.1128/AEM.00611-16},
journal = {Applied and Environmental Microbiology},
number = 15,
volume = 82,
place = {United States},
year = {2016},
month = {5}
}

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    Works referencing / citing this record:

    What do we know about biological nitrogen fixation in insects? Evidence and implications for the insect and the ecosystem
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