skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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:
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)
OSTI Identifier:
1342658
Alternate Identifier(s):
OSTI ID: 1342680; OSTI ID: 1375465
Grant/Contract Number:
AC05-00OR22725; AC02-05CH11231
Resource Type:
Journal Article: 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.
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. Wed . "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 = {Wed Jan 11 00:00:00 EST 2017},
month = {Wed Jan 11 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10works
Citation information provided by
Web of Science

Save / Share:
  • 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 primarymore » 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.« less
  • Cited by 12
  • In this study, Fructobacillus spp. in fructose-rich niches belong to the family Leuconostocaceae. They were originally classified as Leuconostoc spp., but were later grouped into a novel genus, Fructobacillus , based on their phylogenetic position, morphology and specific biochemical characteristics. The unique characters, so called fructophilic characteristics, had not been reported in the group of lactic acid bacteria, suggesting unique evolution at the genome level. Here we studied four draft genome sequences of Fructobacillus spp. and compared their metabolic properties against those of Leuconostoc spp. As a result, Fructobacillus species possess significantly less protein coding sequences in their small genomes.more » The number of genes was significantly smaller in carbohydrate transport and metabolism. Several other metabolic pathways, including TCA cycle, ubiquinone and other terpenoid-quinone biosynthesis and phosphotransferase systems, were characterized as discriminative pathways between the two genera. The adhE gene for bifunctional acetaldehyde/alcohol dehydrogenase, and genes for subunits of the pyruvate dehydrogenase complex were absent in Fructobacillus spp. The two genera also show different levels of GC contents, which are mainly due to the different GC contents at the third codon position. In conclusion, the present genome characteristics in Fructobacillus spp. suggest reductive evolution that took place to adapt to specific niches.« less
  • Ecteinascidin 743 (ET-743, Yondelis) is a clinically approved chemotherapeutic natural product isolated from the Caribbean mangrove tunicate Ecteinascidia turbinata. Researchers have long suspected that a microorganism may be the true producer of the anti-cancer drug, but its genome has remained elusive due to our inability to culture the bacterium in the laboratory using standard techniques. Here, we sequenced and assembled the complete genome of the ET-743 producer, Candidatus Endoecteinascidia frumentensis, directly from metagenomic DNA isolated from the tunicate. Analysis of the ~631 kb microbial genome revealed strong evidence of an endosymbiotic lifestyle and extreme genome reduction. Phylogenetic analysis suggested thatmore » the producer of the anti-cancer drug is taxonomically distinct from other sequenced microorganisms and could represent a new family of Gammaproteobacteria. The complete genome has also greatly expanded our understanding of ET-743 production and revealed new biosynthetic genes dispersed across more than 173 kb of the small genome. The gene cluster’s architecture and its preservation demonstrate that the drug is likely essential to the interactions of the microorganism with its mangrove tunicate host. In conclusion, taken together, these studies elucidate the lifestyle of a unique, and pharmaceutically-important microorganism and highlight the wide diversity of bacteria capable of making potent natural products.« less