Publications

4454

Huanglongbing (HLB), a destructive citrus disease, is associated with ‘Candidatus Liberibacter asiaticus’, which is transmitted by the Asian citrus psyllid Diaphorina citri. Both ‘Ca. L. asiaticus’ and its vector manipulate the host metabolism for their benefit, to meet their nutritional needs and neutralize the host defense responses. We used a targeted gas chromatography-mass spectrometry–based method to explore the connection between the tricarboxylic acid (TCA) cycle, γ-aminobutyric acid (GABA) shunt, and polyamines (PAs) pathways in citrus. ‘Ca. L. asiaticus’ and D. citri accelerated the conversion of α-ketoglutarate to glutamate, then to GABA, causing an accumulation of GABA in the cytosol. In silico analysis showed that the citrus genome possesses a putative GABA permease that connects the GABA shunt with the TCA cycle and supports the accumulation of succinate, fumarate, and citrate. Additionally, the PAs biosynthetic pathway might be connected directly to the TCA cycle, through the production of fumarate, or indirectly, via enhancement of GABA shunt. Taken together, we suggest that GABA shunt and PAs pathways are alternative pathways that contribute to the flux toward succinate rather than an intact TCA cycle in citrus. Both ‘Ca. L. asiaticus’ and its vector enhance these pathways. This study provides more insights into citrus responses to the HLB pathosystem and could be a further step toward clues for understanding the nutritional needs of ‘Ca. L. asiaticus’, which could help in culturing ‘Ca. L. asiaticus’.

Abstract Lucinidae clams harbor gammaproteobacterial thioautotrophic gill endosymbionts that are environmentally acquired. Thioautotrophic lucinid symbionts are related to metabolically similar symbionts associated with diverse marine host taxa and fall into three distinct phylogenetic clades. Most studies on the lucinid–bacteria chemosymbiosis have been done with seagrass-dwelling hosts, whose symbionts belong to the largest phylogenetic clade. In this study, we examined the taxonomy and functional repertoire of bacterial endosymbionts at an unprecedented resolution from Phacoides pectinatus retrieved from mangrove-lined coastal sediments, which are underrepresented in chemosymbiosis studies. The P. pectinatus thioautotrophic endosymbiont expressed metabolic gene variants for thioautotrophy, respiration, and nitrogen assimilation distinct from previously characterized lucinid thioautotrophic symbionts and other marine symbionts. At least two other bacterial species with different metabolisms were also consistently identified in the P. pectinatus gill microbiome, including a Kistimonas-like species and a Spirochaeta-like species. Bacterial transcripts involved in adhesion, growth, and virulence and mixotrophy were highly expressed, as were host-related hemoglobin and lysozyme transcripts indicative of sulfide/oxygen/CO2 transport and bactericidal activity. This study suggests the potential roles of P. pectinatus and its gill microbiome species in mangrove sediment biogeochemistry and offers insights into host and microbe metabolisms in the habitat.