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Title: Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Abstract

One defining feature of cellular evolution is endosymbiosis of bacteria by eukaryotes. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. Furthermore, the genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Our experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata – M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [6];  [6];  [6];  [6];  [7];  [7];  [8];  [9];  [9];  [10];  [11];  [11];  [11] more »;  [11];  [11];  [11];  [4];  [3];  [3];  [3];  [11];  [7];  [1];  [6] « less
+ Show Author Affiliations
  1. Duke Univ., Durham, NC (United States). Dept. of Biology
  2. LF Lambert Spawn Company, Coatesville, PA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  4. Univ. of California, Berkeley, CA (United States)
  5. Arizona State Univ., Tempe, AZ (United States)
  6. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  7. Univ. of Lorraine, Nancy (France). National Inst. for Agricultural Research
  8. Goethe Univ., Frankfurt (Germany). Inst. for Molecular Biosciences
  9. Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France). Architecture and Function of Biological Molecules
  10. Utrecht Univ., (The Netherlands). Dept. of Biology
  11. Joint Genome Inst., Oakland CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1342658
Alternate Identifier(s):
OSTI ID: 1342680; OSTI ID: 1375465
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 19; Journal Issue: 8; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Mortierella elongata; Bacterial Endosymbiosis; Mycoavidus cysteinexigens

Citation Formats

Uehling, J., Gryganskyi, A., Hameed, K., Tschaplinski, T., Misztal, P. K., Wu, S., Desirò, A., Vande Pol, N., Du, Z., Zienkiewicz, A., Zienkiewicz, K., Morin, E., Tisserant, E., Splivallo, R., Hainaut, M., Henrissat, B., Ohm, R., Kuo, A., Yan, J., Lipzen, A., Nolan, M., LaButti, K., Barry, K., Goldstein, A. H., Labbé, J., Schadt, C., Tuskan, G., Grigoriev, I., Martin, F., Vilgalys, R., and Bonito, G. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. United States: N. p., 2017. Web. doi:10.1111/1462-2920.13669.
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Uehling, J., Gryganskyi, A., Hameed, K., Tschaplinski, T., Misztal, P. K., Wu, S., Desirò, A., Vande Pol, N., Du, Z., Zienkiewicz, A., Zienkiewicz, K., Morin, E., Tisserant, E., Splivallo, R., Hainaut, M., Henrissat, B., Ohm, R., Kuo, A., Yan, J., Lipzen, A., Nolan, M., LaButti, K., Barry, K., Goldstein, A. H., Labbé, J., Schadt, C., Tuskan, G., Grigoriev, I., Martin, F., Vilgalys, R., & Bonito, G. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. United States. https://doi.org/10.1111/1462-2920.13669
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Uehling, J., Gryganskyi, A., Hameed, K., Tschaplinski, T., Misztal, P. K., Wu, S., Desirò, A., Vande Pol, N., Du, Z., Zienkiewicz, A., Zienkiewicz, K., Morin, E., Tisserant, E., Splivallo, R., Hainaut, M., Henrissat, B., Ohm, R., Kuo, A., Yan, J., Lipzen, A., Nolan, M., LaButti, K., Barry, K., Goldstein, A. H., Labbé, J., Schadt, C., Tuskan, G., Grigoriev, I., Martin, F., Vilgalys, R., and Bonito, G. Wed . "Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens". United States. https://doi.org/10.1111/1462-2920.13669. https://www.osti.gov/servlets/purl/1342658.
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@article{osti_1342658,
title = {Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens},
author = {Uehling, J. and Gryganskyi, A. and Hameed, K. and Tschaplinski, T. and Misztal, P. K. and Wu, S. and Desirò, A. and Vande Pol, N. and Du, Z. and Zienkiewicz, A. and Zienkiewicz, K. and Morin, E. and Tisserant, E. and Splivallo, R. and Hainaut, M. and Henrissat, B. and Ohm, R. and Kuo, A. and Yan, J. and Lipzen, A. and Nolan, M. and LaButti, K. and Barry, K. and Goldstein, A. H. and Labbé, J. and Schadt, C. and Tuskan, G. and Grigoriev, I. and Martin, F. and Vilgalys, R. and Bonito, G.},
abstractNote = {One defining feature of cellular evolution is endosymbiosis of bacteria by eukaryotes. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. Furthermore, the genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Our experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata – M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.},
doi = {10.1111/1462-2920.13669},
journal = {Environmental Microbiology},
number = 8,
volume = 19,
place = {United States},
year = {Wed Jan 11 00:00:00 EST 2017},
month = {Wed Jan 11 00:00:00 EST 2017}
}
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https://doi.org/10.1111/1462-2920.13669
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    • Li, Fang; Chen, Lin; Redmile-Gordon, Marc
    • Land Degradation & Development, Vol. 29, Issue 6
    • DOI: 10.1002/ldr.2965

    Bacterial quorum sensing in symbiotic and pathogenic relationships with hosts
    journal, February 2018

    Bacterial–fungal interactions: ecology, mechanisms and challenges
    journal, February 2018

    • Deveau, Aurélie; Bonito, Gregory; Uehling, Jessie
    • FEMS Microbiology Reviews, Vol. 42, Issue 3
    • DOI: 10.1093/femsre/fuy008

    Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle
    journal, February 2018

    Cytosolic lipid droplets as engineered organelles for production and accumulation of terpenoid biomaterials in leaves
    journal, February 2019

    Unveiling Concealed Functions of Endosymbiotic Bacteria Harbored in the Ascomycete Stachylidium bicolor
    journal, June 2018

    • Almeida, Celso; Silva Pereira, Cristina; Gonzalez-Menendez, Victor
    • Applied and Environmental Microbiology, Vol. 84, Issue 15
    • DOI: 10.1128/aem.00660-18

    Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi
    journal, April 2018

    • Field, Katie J.; Pressel, Silvia
    • New Phytologist, Vol. 220, Issue 4
    • DOI: 10.1111/nph.15158

    Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina
    journal, February 2019

    • Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène
    • New Phytologist, Vol. 222, Issue 3
    • DOI: 10.1111/nph.15687

    Increasing access to microfluidics for studying fungi and other branched biological structures
    journal, June 2019

    • Millet, Larry J.; Aufrecht, Jayde; Labbé, Jessy
    • Fungal Biology and Biotechnology, Vol. 6, Issue 1
    • DOI: 10.1186/s40694-019-0071-z

    At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions
    journal, October 2019

    • Venice, Francesco; Ghignone, Stefano; Salvioli di Fossalunga, Alessandra
    • Environmental Microbiology, Vol. 22, Issue 1
    • DOI: 10.1111/1462-2920.14827

    Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata
    journal, June 2018

    The fungal holobiont: Evidence from early diverging fungi
    journal, April 2017

    Cytosolic lipid droplets as engineered organelles for production and accumulation of terpenoid biomaterials in leaves
    journal, February 2019

    Increasing access to microfluidics for studying fungi and other branched biological structures
    journal, June 2019

    • Millet, Larry J.; Aufrecht, Jayde; Labbé, Jessy
    • Fungal Biology and Biotechnology, Vol. 6, Issue 1
    • DOI: 10.1186/s40694-019-0071-z

    Aposymbiosis of a Burkholderiaceae-Related Endobacterium Impacts on Sexual Reproduction of Its Fungal Host
    journal, January 2020

    • Takashima, Yusuke; Degawa, Yousuke; Nishizawa, Tomoyasu
    • Microbes and Environments, Vol. 35, Issue 2
    • DOI: 10.1264/jsme2.me19167

    Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems
    journal, October 2017

    Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange
    journal, October 2019

    • Uehling, Jessie K.; Entler, Matthew R.; Meredith, Hannah R.
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.02163

    Algae and fungi move from the past to the future
    journal, July 2019

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