Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon
ABSTRACT Loss of flagellar genes causes a nonmotile phenotype. The genus Lysobacter consists of numerous environmentally ubiquitous, nonflagellated bacteria, including Lysobacter enzymogenes, an antifungal bacterium that is beneficial to plants. L. enzymogenes still has many flagellar genes on its g...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-02-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.04149-22 |
| _version_ | 1828033528580800512 |
|---|---|
| author | Dan Xiong Zixiang Yang Xueting He Weimei He Danyu Shen Lu Wang Long Lin Aprodisia Murero Tohru Minamino Xiaolong Shao Guoliang Qian |
| author_facet | Dan Xiong Zixiang Yang Xueting He Weimei He Danyu Shen Lu Wang Long Lin Aprodisia Murero Tohru Minamino Xiaolong Shao Guoliang Qian |
| author_sort | Dan Xiong |
| collection | DOAJ |
| description | ABSTRACT Loss of flagellar genes causes a nonmotile phenotype. The genus Lysobacter consists of numerous environmentally ubiquitous, nonflagellated bacteria, including Lysobacter enzymogenes, an antifungal bacterium that is beneficial to plants. L. enzymogenes still has many flagellar genes on its genome, although this bacterium does not engage in flagella-driven motility. Here, we report that loss of certain flagellar genes allows L. enzymogenes to strengthen its evolutionarily gained capacity in fungal killing. To clarify why this bacterium loses flagellar genes during the evolutionary process, we cloned several representative flagellar genes from Xanthomonas oryzae, a flagellated, phylogenetically related species of Lysobacter, and introduced them individually into L. enzymogenes to mimic genomic reacquisition of lost flagellar genes. Heterogeneous expression of the three X. oryzae flagellar structural genes (Xo-motA, Xo-motB, Xo-fliE) and one flagellar regulatory gene (Xo-fleQ) remarkably weakened the bacterial capacity to kill fungal pathogens by impairing the synthesis of an antifungal weapon, known as the heat-stable antifungal factor (HSAF). We further investigated the underlying mechanism by selecting Xo-FleQ as the representative because it is a master transcription factor responsible for flagellar gene expression. Xo-FleQ inhibited the transcription of operon genes responsible for HSAF synthesis via direct binding of Xo-FleQ to the promoter region, thereby decreasing HSAF biosynthesis by L. enzymogenes. These observations suggest a possible genome and function coevolution event, in which an antifungal bacterium deletes certain flagellar genes in order to enhance its ability to kill fungi. IMPORTANCE It is generally recognized that flagellar genes are commonly responsible for the flagella-driven bacterial motility. Thus, finding nonflagellated bacteria partially or fully lost flagellar genes is not a surprise. However, the present study provides new insights into this common idea. We found that loss of either certain flagellar structural or regulatory genes (such as motA, motB, fliE, and fleQ) allows a nonflagellated, antifungal bacterium (L. enzymogenes) to stimulate its fungal-killing capacity, outlining a genome-function coevolution event, where an antifungal bacterium “smartly” designed its genome to “delete” crucial flagellar genes to coordinate flagellar loss and fungal predation. This unusual finding might trigger bacteriologists to reconsider previously ignored functions of the lost flagellar genes in any nonflagellated, pathogenic, or beneficial bacteria. |
| first_indexed | 2024-04-10T15:21:00Z |
| format | Article |
| id | doaj.art-e34131250aff474f9020a21e46c89012 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-10T15:21:00Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-e34131250aff474f9020a21e46c890122023-02-14T14:15:50ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.04149-22Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal WeaponDan Xiong0Zixiang Yang1Xueting He2Weimei He3Danyu Shen4Lu Wang5Long Lin6Aprodisia Murero7Tohru Minamino8Xiaolong Shao9Guoliang Qian10College of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaMedical College, China Three Gorges University, Yichang, ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaGraduate School of Frontier Biosciences, Osaka University, Suita, Osaka, JapanCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaCollege of Plant Protection, State Key Laboratory of Biological Interactions and Crop Health, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, P. R. ChinaABSTRACT Loss of flagellar genes causes a nonmotile phenotype. The genus Lysobacter consists of numerous environmentally ubiquitous, nonflagellated bacteria, including Lysobacter enzymogenes, an antifungal bacterium that is beneficial to plants. L. enzymogenes still has many flagellar genes on its genome, although this bacterium does not engage in flagella-driven motility. Here, we report that loss of certain flagellar genes allows L. enzymogenes to strengthen its evolutionarily gained capacity in fungal killing. To clarify why this bacterium loses flagellar genes during the evolutionary process, we cloned several representative flagellar genes from Xanthomonas oryzae, a flagellated, phylogenetically related species of Lysobacter, and introduced them individually into L. enzymogenes to mimic genomic reacquisition of lost flagellar genes. Heterogeneous expression of the three X. oryzae flagellar structural genes (Xo-motA, Xo-motB, Xo-fliE) and one flagellar regulatory gene (Xo-fleQ) remarkably weakened the bacterial capacity to kill fungal pathogens by impairing the synthesis of an antifungal weapon, known as the heat-stable antifungal factor (HSAF). We further investigated the underlying mechanism by selecting Xo-FleQ as the representative because it is a master transcription factor responsible for flagellar gene expression. Xo-FleQ inhibited the transcription of operon genes responsible for HSAF synthesis via direct binding of Xo-FleQ to the promoter region, thereby decreasing HSAF biosynthesis by L. enzymogenes. These observations suggest a possible genome and function coevolution event, in which an antifungal bacterium deletes certain flagellar genes in order to enhance its ability to kill fungi. IMPORTANCE It is generally recognized that flagellar genes are commonly responsible for the flagella-driven bacterial motility. Thus, finding nonflagellated bacteria partially or fully lost flagellar genes is not a surprise. However, the present study provides new insights into this common idea. We found that loss of either certain flagellar structural or regulatory genes (such as motA, motB, fliE, and fleQ) allows a nonflagellated, antifungal bacterium (L. enzymogenes) to stimulate its fungal-killing capacity, outlining a genome-function coevolution event, where an antifungal bacterium “smartly” designed its genome to “delete” crucial flagellar genes to coordinate flagellar loss and fungal predation. This unusual finding might trigger bacteriologists to reconsider previously ignored functions of the lost flagellar genes in any nonflagellated, pathogenic, or beneficial bacteria.https://journals.asm.org/doi/10.1128/spectrum.04149-22L. enzymogenesflagellaFleQHSAFevolutionenvironmental microbiology |
| spellingShingle | Dan Xiong Zixiang Yang Xueting He Weimei He Danyu Shen Lu Wang Long Lin Aprodisia Murero Tohru Minamino Xiaolong Shao Guoliang Qian Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon Microbiology Spectrum L. enzymogenes flagella FleQ HSAF evolution environmental microbiology |
| title | Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon |
| title_full | Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon |
| title_fullStr | Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon |
| title_full_unstemmed | Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon |
| title_short | Loss of Flagella-Related Genes Enables a Nonflagellated, Fungal-Predating Bacterium To Strengthen the Synthesis of an Antifungal Weapon |
| title_sort | loss of flagella related genes enables a nonflagellated fungal predating bacterium to strengthen the synthesis of an antifungal weapon |
| topic | L. enzymogenes flagella FleQ HSAF evolution environmental microbiology |
| url | https://journals.asm.org/doi/10.1128/spectrum.04149-22 |
| work_keys_str_mv | AT danxiong lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT zixiangyang lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT xuetinghe lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT weimeihe lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT danyushen lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT luwang lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT longlin lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT aprodisiamurero lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT tohruminamino lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT xiaolongshao lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon AT guoliangqian lossofflagellarelatedgenesenablesanonflagellatedfungalpredatingbacteriumtostrengthenthesynthesisofanantifungalweapon |