Identification of c-di-GMP Signaling Components in Xanthomonas oryzae and Their Orthologs in Xanthomonads Involved in Regulation of Bacterial Virulence Expression

Abstract

Xanthomonas oryzae pv. oryzae ( Xoo ) causes bacterial leaf blight of rice, one of the most devastating bacterial diseases of this staple crop worldwide. Xoo produces a range of virulence-related factors to facilitate its pathogenesis in rice, however, the regulatory mechanisms of Xoo virulence expression have been not fully elucidated. Recent studies have revealed that virulence factor production is regulated via cyclic dimeric guanosine monophosphate (c-di-GMP) signaling pathway that is well-conserved in Xoo and other Xanthomonas species. A set of GGDEF, EAL, HD-GYP, and PilZ domain proteins with diverse signal sensory domains for c-di-GMP synthesis, hydrolysis, and binding is encoded in the Xoo genome. Bioinformatic, genetic, and biochemical analysis has identified an array of diguanylate cyclases (DGCs) and phosphodiesterases (PDEs), as well as degenerate GGDEF/EAL, PilZ domain proteins along with a transcription regulator. These signaling components have been characterized to regulate various bacterial cellular processes, such as virulence, exopolysaccharide (EPS) production, biofilm formation, motility, and adaptation at the transcriptional, post-translational, and protein-protein interaction levels. This review summarized the recent progress in understanding the importance and complexity of c-di-GMP signaling in regulating bacterial virulence expression, highlighting the identified key signal elements and orthologs found in Xanthomonads, discussing the diverse functions of GGDEF/EAL/HD-GYP domains, existence of a complicated multifactorial network between DGCs, PDEs, and effectors, and further exploration of the new c-di-GMP receptor domains. These findings and knowledge lay the groundwork for future experimentation to further elucidate c-di-GMP regulatory circuits involved in regulation of bacterial pathogenesis.

Quorum Sensing-Independent Cellulase-Sensitive Pellicle Formation Is Critical for Colonization of Burkholderia glumae in Rice Plants

“…Bacterial cellulose facilitates intimate interactions between bacterial cellulose producers and various components present in the environment (Yamamoto et al, 2011). Particularly for plantor animal-associated bacteria, cellulosic biofilms are important for close interactions with their hosts (Pérez-Mendoza et al, 2014;Augimeri et al, 2015;Yang et al, 2019). Formation of bacterial cellulosic pellicle is accomplished by five main proteins encoded by bacterial cellulose biosynthetic (bcs) genes, bcs A, B, C, D, and Z (Saxena et al, 1994;Le Quéré and Ghigo, 2009).…”

Transcriptome Analysis Revealed Overlapping and Special Regulatory Roles of RpoN1 and RpoN2 in Motility, Virulence, and Growth of Xanthomonas oryzae pv. oryzae

“…c-di-GMP, the widespread second messenger in pathogenic bacteria, plays a crucial role in regulating Xoo motility and virulence ( Yang et al, 2019 ). Diguanylate cyclase (DGC) enzyme contains a conserved GGDEF domain, which regulates c-di-GMP synthesis, whereas phosphodiesterase (PDE) enzyme-containing conserved EAL or HD-GYP domains controls c-di-GMP degradation.…”

“…The antagonistic enzymatic actions of DGC and PDE enzymes regulate the synthesis and degradation of intracellular c-di-GMP, respectively. DGCs contain a conserved GGDEF domain, while PDEs contain conserved EAL or HD-GYP domains ( Yang et al, 2019 ). A previous study reported that two GGDEF domain proteins, GdpX1 from Xoo strain PXO99 A and DgcA from Xoo strain KACC10331, negatively regulates bacterial virulence, EPS production, and motility ( Su et al, 2016 ; Yang et al, 2016 ).…”

“…Besides, it is used as an ideal model to study the molecular mechanisms of bacterial pathogenicity in monocot plants ( Nino-Liu et al, 2006 ). Xoo contains several genes related to motility, chemotaxis, EPS, biofilm, and cyclic dimeric guanosine monophosphate (c-di-GMP), controlled by diverse transcriptional factors ( Das et al, 2009 ; White and Yang, 2009 ; Yang et al, 2019 ). Two σ 54 factors, RpoN1 and RpoN2, were identified in Xoo in our previous work ( Tian et al, 2015 ).…”

The Multiple Regulatory Relationship Between RNA-Chaperone Hfq and the Second Messenger c-di-GMP

“…In addition, in several Gram-negative bacteria such as Xanthomonas (Yang et al, 2015(Yang et al, , 2019Lai et al, 2018;Xue et al, 2018;Liu et al, 2019), Vibrio Camilli, 2004, 2005;Liu et al, 2011;Bardill and Hammer, 2012;Zamorano-Sánchez et al, 2019;Wu et al, 2020), and in certain Gram-positive bacteria such as Bacillus (Chen et al, 2012;Fagerlund et al, 2016;Jagtap et al, 2016;Fu et al, 2018), both Hfq and c-di-GMP are found to participate in the regulation of phenotypes such as motility, biofilm formation and virulence, which demonstrate well that both Hfq and c-di-GMP can co-regulate certain phenotype in different bacteria. We thus assume that there is a certain relationship between the Hfq regulatory system and c-di-GMP signal transduction system.…”