Deletion of flgL in Mesorhizobium ciceri USDA 3378 weakened competitive nodulation ability by reducing flagellum formation, biofilm formation, and extracellular polysaccharide secretion.

Authors

Keyu Chen, Cancan Zhu, Ke Li, Haoran Hao, Kaiwen Zhang, Youguo Li, Mitchell Andrews, Junjie Zhang

Published in

Applied and environmental microbiology. Pages e0093126. Jul 10, 2026. Epub Jul 10, 2026.

Abstract

Mesorhizobium ciceri USDA 3378 has a competitive advantage over the indigenous Mesorhizobium muleiense CCBAU 83963 in nodulating chickpea (Cicer arietinum L.) in newly introduced planting areas in China. The underlying mechanisms for this dominance remain unclear. A comparison of the genomes of USDA 3378 and CCBAU 83963 revealed significantly more genes involved in flagellum production and cell movement in USDA 3378. USDA 3378 produced flagella, but CCBAU 83963 did not and showed lower motility, biofilm production, and extracellular polysaccharide secretion than USDA 3378. Transcriptome analysis of USDA 3378 under simulated symbiotic versus non-symbiotic conditions showed strong induction of nodulation genes and a broader transcriptional response among genes assigned to quorum sensing, chemotaxis, and flagellar assembly, with flgL (encoding a flagellar hook-associated family protein) being the only upregulated flagellar structural gene detected. A flgL mutant strain based on USDA 3378 (ΔflgL-3378) showed similar growth to USDA 3378 but was unable to produce flagella and exhibited concomitant reductions in motility, biofilm production, and extracellular polysaccharide secretion. Nodule occupancy by USDA 3378 was 100% when co-inoculated with CCBAU 83963. In contrast, nodule occupancy by ΔflgL-3378 was significantly reduced to 39.88% when co-inoculated with the wild-type USDA 3378. However, when co-inoculated with the indigenous strain CCBAU 83963, ΔflgL-3378 still showed a dominant occupancy of 82.8%. Transcriptome analysis of ΔflgL-3378 under the same comparison showed continued induction of nodulation genes and several flagellar system genes, an altered quorum-sensing-associated response, and no detectable chemotaxis-related differentially expressed genes. We conclude that flgL and flagella act as important contributors to the superior competitive nodulation ability of M. ciceri USDA 3378 over M. muleiense in chickpea, although other intrinsic genomic advantages likely contribute to its basal competitivenessIMPORTANCEChickpea is an important legume crop that depends on symbiotic rhizobia for biological nitrogen fixation. In newly introduced chickpea-growing regions of China, Mesorhizobium ciceri USDA 3378 shows a strong competitive advantage in nodulating chickpea compared with the indigenous strain Mesorhizobium muleiense CCBAU 83963, but the mechanisms underlying this advantage remain unclear. This study identifies the flagellar hook-associated gene flgL as an important contributor to the competitive nodulation ability of USDA 3378. Deletion of flgL abolished flagellum formation and reduced motility, biofilm formation, extracellular polysaccharide production, and competitive nodulation ability. However, the ΔflgL mutant still retained higher competitiveness than CCBAU 83963, indicating that additional motility-independent traits also contribute to the basal competitiveness of USDA 3378. These findings improve our understanding of the bacterial traits that influence rhizobial competitiveness and may help guide the development of more effective chickpea inoculants for diverse agricultural environments.

PMID:
42429764
Bibliographic data and abstract were imported from PubMed on 10 Jul 2026.

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