A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i>
<i>Fusarium</i> trichothecenes are among the mycotoxins of most concern to food and feed safety. Production of these mycotoxins and presence of the trichothecene biosynthetic gene (<i>TRI</i>) cluster have been confirmed in only two multispecies lineages of <i>Fusarium&...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-12-01
|
| Series: | Toxins |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2072-6651/15/1/12 |
| _version_ | 1797436668259598336 |
|---|---|
| author | Robert H. Proctor Guixia Hao Hye-Seon Kim Briana K. Whitaker Imane Laraba Martha M. Vaughan Susan P. McCormick |
| author_facet | Robert H. Proctor Guixia Hao Hye-Seon Kim Briana K. Whitaker Imane Laraba Martha M. Vaughan Susan P. McCormick |
| author_sort | Robert H. Proctor |
| collection | DOAJ |
| description | <i>Fusarium</i> trichothecenes are among the mycotoxins of most concern to food and feed safety. Production of these mycotoxins and presence of the trichothecene biosynthetic gene (<i>TRI</i>) cluster have been confirmed in only two multispecies lineages of <i>Fusarium</i>: the <i>Fusarium incarnatum</i>-<i>equiseti</i> (Incarnatum) and <i>F. sambucinum</i> (Sambucinum) species complexes. Here, we identified and characterized a <i>TRI</i> cluster in a species that has not been formally described and is represented by <i>Fusarium</i> sp. NRRL 66739. This fungus is reported to be a member of a third <i>Fusarium</i> lineage: the <i>F. buharicum</i> species complex. Cultures of NRRL 66739 accumulated only two trichothecenes, 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol. Although these are not novel trichothecenes, the production profile of NRRL 66739 is novel, because in previous reports 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol were components of mixtures of 6–8 trichothecenes produced by several <i>Fusarium</i> species in Sambucinum. Heterologous expression analysis indicated that the <i>TRI13</i> gene in NRRL 66739 confers trichothecene 7-hydroxylation. This contrasts the trichothecene 4-hydroxylation function of <i>TRI13</i> in other <i>Fusarium</i> species. Phylogenetic analyses suggest that NRRL 66739 acquired the <i>TRI</i> cluster via horizontal gene transfer from a close relative of Incarnatum and Sambucinum. These findings provide insights into evolutionary processes that have shaped the distribution of trichothecene production among <i>Fusarium</i> species and the structural diversity of the toxins. |
| first_indexed | 2024-03-09T11:05:54Z |
| format | Article |
| id | doaj.art-25cdbfb0133346278c286bace3ecf225 |
| institution | Directory Open Access Journal |
| issn | 2072-6651 |
| language | English |
| last_indexed | 2024-03-09T11:05:54Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Toxins |
| spelling | doaj.art-25cdbfb0133346278c286bace3ecf2252023-12-01T00:56:26ZengMDPI AGToxins2072-66512022-12-011511210.3390/toxins15010012A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i>Robert H. Proctor0Guixia Hao1Hye-Seon Kim2Briana K. Whitaker3Imane Laraba4Martha M. Vaughan5Susan P. McCormick6Mycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USAMycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USAMycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USAMycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USAOak Ridge Institute for Science and Education, Mycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USAMycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USAMycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USA<i>Fusarium</i> trichothecenes are among the mycotoxins of most concern to food and feed safety. Production of these mycotoxins and presence of the trichothecene biosynthetic gene (<i>TRI</i>) cluster have been confirmed in only two multispecies lineages of <i>Fusarium</i>: the <i>Fusarium incarnatum</i>-<i>equiseti</i> (Incarnatum) and <i>F. sambucinum</i> (Sambucinum) species complexes. Here, we identified and characterized a <i>TRI</i> cluster in a species that has not been formally described and is represented by <i>Fusarium</i> sp. NRRL 66739. This fungus is reported to be a member of a third <i>Fusarium</i> lineage: the <i>F. buharicum</i> species complex. Cultures of NRRL 66739 accumulated only two trichothecenes, 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol. Although these are not novel trichothecenes, the production profile of NRRL 66739 is novel, because in previous reports 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol were components of mixtures of 6–8 trichothecenes produced by several <i>Fusarium</i> species in Sambucinum. Heterologous expression analysis indicated that the <i>TRI13</i> gene in NRRL 66739 confers trichothecene 7-hydroxylation. This contrasts the trichothecene 4-hydroxylation function of <i>TRI13</i> in other <i>Fusarium</i> species. Phylogenetic analyses suggest that NRRL 66739 acquired the <i>TRI</i> cluster via horizontal gene transfer from a close relative of Incarnatum and Sambucinum. These findings provide insights into evolutionary processes that have shaped the distribution of trichothecene production among <i>Fusarium</i> species and the structural diversity of the toxins.https://www.mdpi.com/2072-6651/15/1/12trichothecenemycotoxinsecondary metabolite<i>Fusarium</i>biosynthetic gene clusterhorizontal gene transfer |
| spellingShingle | Robert H. Proctor Guixia Hao Hye-Seon Kim Briana K. Whitaker Imane Laraba Martha M. Vaughan Susan P. McCormick A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> Toxins trichothecene mycotoxin secondary metabolite <i>Fusarium</i> biosynthetic gene cluster horizontal gene transfer |
| title | A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> |
| title_full | A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> |
| title_fullStr | A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> |
| title_full_unstemmed | A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> |
| title_short | A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in <i>Fusarium</i> |
| title_sort | novel trichothecene toxin phenotype associated with horizontal gene transfer and a change in gene function in i fusarium i |
| topic | trichothecene mycotoxin secondary metabolite <i>Fusarium</i> biosynthetic gene cluster horizontal gene transfer |
| url | https://www.mdpi.com/2072-6651/15/1/12 |
| work_keys_str_mv | AT roberthproctor anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT guixiahao anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT hyeseonkim anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT brianakwhitaker anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT imanelaraba anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT marthamvaughan anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT susanpmccormick anoveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT roberthproctor noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT guixiahao noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT hyeseonkim noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT brianakwhitaker noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT imanelaraba noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT marthamvaughan noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi AT susanpmccormick noveltrichothecenetoxinphenotypeassociatedwithhorizontalgenetransferandachangeingenefunctioninifusariumi |