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

Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. 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. Furthermore, 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. 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. 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. In independent comparative phylogenomic analyses of fungal and bacterial genomes we find that they 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
  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:
Grant/Contract Number:
AC05-00OR22725; AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 19; Journal Issue: 8; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Mortierella elongata; Bacterial Endosymbiosis; Mycoavidus cysteinexigens
OSTI Identifier:
1342658
Alternate Identifier(s):
OSTI ID: 1342680; OSTI ID: 1375465

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., Web. doi:10.1111/1462-2920.13669.
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. doi:10.1111/1462-2920.13669.
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.. 2017. "Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens". United States. doi:10.1111/1462-2920.13669. https://www.osti.gov/servlets/purl/1342658.
@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 = {Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. 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. Furthermore, 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. 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. 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. In independent comparative phylogenomic analyses of fungal and bacterial genomes we find that they 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 = {2017},
month = {1}
}

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