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Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria Raimund Nagel Iowa State University, [email protected]

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Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria Raimund Nagel Iowa State University, Rnagel@Iastate.Edu Biochemistry, Biophysics and Molecular Biology Biochemistry, Biophysics and Molecular Biology Publications 11-2018 A Third Class: Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria Raimund Nagel Iowa State University, [email protected] John E. Bieber Iowa State University Mark G. Schmidt-Dannert Iowa State University, [email protected] Ryan S. Nett Iowa State University Reuben J. Peters Iowa State University, [email protected] Follow this and additional works at: https://lib.dr.iastate.edu/bbmb_ag_pubs Part of the Biochemistry, Biophysics, and Structural Biology Commons, Microbiology Commons, and the Plant Biology Commons The ompc lete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ bbmb_ag_pubs/202. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Biochemistry, Biophysics and Molecular Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Biochemistry, Biophysics and Molecular Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. A Third Class: Functional Gibberellin Biosynthetic Operon in Beta- Proteobacteria Abstract The ba ility of plant-associated microbes to produce gibberellin A (GA) phytohormones was first described for the fungal rice pathogen Gibberella fujikuroi in the 1930s. Recently the capacity to produce GAs was shown for several bacteria, including symbiotic alpha-proteobacteria (α-rhizobia) and gamma-proteobacteria phytopathogens. All necessary enzymes for GA production are encoded by a conserved operon, which appears to have undergone horizontal transfer between and within these two phylogenetic classes of bacteria. Here the operon was shown to be present and functional in a third class, the beta-proteobacteria, where it is found in several symbionts (β-rhizobia). Conservation of function was examined by biochemical characterization of the enzymes encoded by the operon from Paraburkholderia mimosarum LMG 23256T. Despite the in-frame gene fusion between the short-chain alcohol dehydrogenase/reductase and ferredoxin, the encoded enzymes exhibited the expected activity. Intriguingly, together these can only produce GA9, the immediate precursor to the bioactive GA4, as the cytochrome P450 (CYP115) that catalyzes the final hydroxylation reaction is missing, similar to most α-rhizobia. However, phylogenetic analysis indicates that the operon from β-rhizobia is more closely related to examples from gamma-proteobacteria, which almost invariably have CYP115 and, hence, can produce bioactive GA4. This indicates not only that β-rhizobia acquired the operon by horizontal gene transfer from gamma-proteobacteria, rather than α-rhizobia, but also that they independently lost CYP115 in parallel to the α-rhizobia, further hinting at the possibility of detrimental effects for the production of bioactive GA4 by these symbionts. Keywords symbiosis, gibberellin, rhizobia, legume (nodules), evolution Disciplines Biochemistry, Biophysics, and Structural Biology | Microbiology | Plant Biology Comments This article is published as Nagel, Raimund, John E. Bieber, Mark G. Schmidt-Dannert, Ryan S. Nett, and Reuben J. Peters. "A third class: Functional gibberellin biosynthetic operon in beta-proteobacteria." Frontiers in Microbiology 9 (2018): 2916. doi: 10.3389/fmicb.2018.02916. Creative Commons License This work is licensed under a Creative Commons Attribution 4.0 License. This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/bbmb_ag_pubs/202 fmicb-09-02916 November 27, 2018 Time: 13:59 # 1 ORIGINAL RESEARCH published: 27 November 2018 doi: 10.3389/fmicb.2018.02916 A Third Class: Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria Raimund Nagel1, John E. Bieber1,2, Mark G. Schmidt-Dannert1, Ryan S. Nett1 and Reuben J. Peters1* 1 Roy J. Carver Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State University, Ames, IA, United States, 2 Science Department, Newton Senior High School, Newton, IA, United States The ability of plant-associated microbes to produce gibberellin A (GA) phytohormones was first described for the fungal rice pathogen Gibberella fujikuroi in the 1930s. Recently the capacity to produce GAs was shown for several bacteria, including symbiotic alpha-proteobacteria (a-rhizobia) and gamma-proteobacteria phytopathogens. All necessary enzymes for GA production are encoded by a conserved operon, which appears to have undergone horizontal transfer between and within these two phylogenetic classes of bacteria. Here the operon was shown to be present and functional in a third class, the beta-proteobacteria, where it is found in Edited by: Eloise Foo, several symbionts (b-rhizobia). Conservation of function was examined by biochemical University of Tasmania, Australia characterization of the enzymes encoded by the operon from Paraburkholderia Reviewed by: mimosarum LMG 23256T. Despite the in-frame gene fusion between the short-chain Maria Jose Soto, Spanish National Research Council alcohol dehydrogenase/reductase and ferredoxin, the encoded enzymes exhibited the (CSIC), Spain expected activity. Intriguingly, together these can only produce GA9, the immediate Yuri A. Trotsenko, precursor to the bioactive GA , as the cytochrome P450 (CYP115) that catalyzes the Institute of Biochemistry 4 and Physiology of Microorganisms final hydroxylation reaction is missing, similar to most a-rhizobia. However, phylogenetic (RAS), Russia analysis indicates that the operon from b-rhizobia is more closely related to examples *Correspondence: from gamma-proteobacteria, which almost invariably have CYP115 and, hence, can Reuben J. Peters [email protected] produce bioactive GA4. This indicates not only that b-rhizobia acquired the operon by horizontal gene transfer from gamma-proteobacteria, rather than a-rhizobia, but also Specialty section: that they independently lost CYP115 in parallel to the a-rhizobia, further hinting at the This article was submitted to Plant Microbe Interactions, possibility of detrimental effects for the production of bioactive GA4 by these symbionts. a section of the journal Keywords: symbiosis, gibberellin, rhizobia, legume (nodules), evolution Frontiers in Microbiology Received: 14 September 2018 Accepted: 13 November 2018 Published: 27 November 2018 INTRODUCTION Citation: Nagel R, Bieber JE, Gibberellin A (GA) was first discovered in the eponymous fungal rice pathogen Gibberella Schmidt-Dannert MG, Nett RS and fujikuroi, which eventually enabled identification of these diterpenoids in plants where they serve Peters RJ (2018) A Third Class: Functional Gibberellin Biosynthetic as hormones regulating growth and development (Hedden and Sponsel, 2015). As suggested Operon in Beta-Proteobacteria. from their production by G. fujikuroi, these phytohormones also affect plant-microbe interactions Front. Microbiol. 9:2916. (De Bruyne et al., 2014). However, in bacteria GA production was first reported from nitrogen- doi: 10.3389/fmicb.2018.02916 fixing rhizobial symbionts rather than plant pathogens (Bottini et al., 2004). Frontiers in Microbiology| www.frontiersin.org 1 November 2018| Volume 9| Article 2916 fmicb-09-02916 November 27, 2018 Time: 13:59 # 2 Nagel et al. Gibberellin Biosynthetic Operon in Beta-Proteobacteria More recently, bacterial GA biosynthesis has been elucidated By contrast, phytopathogens can produce the bioactive GA4. (Morrone et al., 2009; Hershey et al., 2014; Lu et al., 2015; This difference in final GA product presumably reflects their Tatsukami and Ueda, 2016; Nagel and Peters, 2017b; Nagel et al., distinct relationships with plant hosts. While it has been noted 2017; Nett et al., 2017b), with all the necessary genes generally that a symbiotic beta-proteobacteria (b-rhizobia) also contains found in close association within a biosynthetic operon. This the operon (Nagel and Peters, 2017b), this has not otherwise been operon seems to only be found in plant-associated bacteria (Levy investigated. The genome of Paraburkholderia mimosarum LMG et al., 2017). However, beyond the symbiotic alpha-proteobacteria 23256T contains the core operon necessary for GA biosynthesis. (a-rhizobia) where the operon was originally reported and This b-rhizobium was isolated from Mimosa pigra and shown characterized (Tully and Keister, 1993; Tully et al., 1998; Keister to form indeterminate nodules with its host (Chen et al., et al., 1999; Morrone et al., 2009; Hershey et al., 2014; Tatsukami 2005, 2006). Here the enzymes encoded by the operon from and Ueda, 2016; Nett et al., 2017b), the operon also was found P. mimosarum LMG 23256T were characterized and shown to to be functionally present in a diverse group of plant pathogens be functionally conserved, with further phylogenetic analysis from the gamma-proteobacteria class (Lu et al., 2015; Nagel indicating not only independent acquisition of the operon from and Peters, 2017b; Nagel et al., 2017). Indeed, there is greater gamma-proteobacteria, but also loss of CYP115, which supports phylogenetic diversity of the operon in these phytopathogens the hypothesis that direct production of bioactive GA4 may have than rhizobia (Nagel and Peters, 2017b), suggesting that bacterial a deleterious effect in the symbiotic relationship between rhizobia GA biosynthesis originally evolved in this distinct class of and
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