Unveiling metabolic integration in psyllids and their nutritional endosymbionts through comparative transcriptomics analysis

Kwak, Younghwan; Hansen, Allison K.

doi:10.1016/j.isci.2023.107930

Cited by 5 publications

(5 citation statements)

References 92 publications

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“…2 ). This arrangement potentially facilitates the delivery of proteins and metabolites required to maintain the bacteriocyte symbiosis, being consistent with metabolic complementarity between the host and Carsonella , which was suggested by genomic and transcriptomic analyses ( 8 , 16 , 18 – 20 , 36 ). In the case of aphids, sternorrhynchan insects closely related to psyllids, proteins synthesized by the host bacteriocytes are shown to be transported to the endosymbiont ( 62 ).…”

Section: Discussionsupporting

confidence: 74%

“…Besides, limited numbers of Wolbachia cells were observed in the uninucleate bacteriocytes ( Fig. 1G, H and I ), which potentially allow Wolbachia to enjoy the environment of the bacteriocyte, where various metabolites are assumed to be actively synthesized and transferred among the host and symbionts ( 16 , 36 ). However, previous analyses showed that the relative abundance of Wolbachia was much higher in Malpighian tubules and the gut ( 43 ), implying that the bacteriome is not the best habitat for Wolbachia .…”

Section: Discussionmentioning

confidence: 99%

“…The metabolic genes encoded in the Profftella genome are largely nonredundant with those of Carsonella , indicating complementarity between these symbionts ( 8 ). Furthermore, many host genes are upregulated in the bacteriome to complement the incomplete biosynthetic pathways deduced from the highly reduced Carsonella genome ( 16 , 36 ). The majority of them are native animal genes, but some are shown to be of bacterial origin, which the host psyllid has horizontally acquired.…”

Section: Introductionmentioning

confidence: 99%

“…An ortholog is retained in the Carsonella genome but appears to have acquired a novel function independent of arginine biosynthesis. Another notable example is a gene ( ribC ) involved in the biosynthesis of riboflavin or vitamin B 2 ( 16 , 36 ), which is also scarce in the phloem sap diet ( 22 ). Although Profftella lacks most genes for nutritional provisioning, it exceptionally retains all genes for the riboflavin biosynthetic pathway other than ribC ( 8 ), suggesting metabolic complementarity between Profftella and the host psyllid ( 16 ).…”

Section: Introductionmentioning

confidence: 99%

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Ultrastructure of the bacteriome and bacterial symbionts in the Asian citrus psyllid, Diaphorina citri

Nakabachi,

Suzaki

2024

Microbiol Spectr

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The Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) is a notorious agricultural pest that transmits “ Candidatus Liberibacter” spp. (Alphaproteobacteria: Rhizobiales ), the pathogens of the destructive citrus disease huanglongbing. D. citri possesses a specialized organ called the bacteriome, consisting of uninucleate bacteriocytes and a syncytium. The bacteriocytes harbor “ Candidatus Carsonella ruddii” (Gammaproteobacteria: Oceanospirillales ), a nutritional symbiont that provides essential amino acids scarce in the phloem sap diet. The syncytium contains “ Candidatus Profftella armatura” (Gammaproteobacteria: Burkholderiales ), a defensive symbiont synthesizing diaphorin, a polyketide inhibitory to various organisms. Besides these obligate mutualists, Wolbachia (Alphaproteobacteria: Rickettsiales ), a facultative symbiont, is also widespread in D. citri . To understand the morphological features of the bacteriome and symbionts, this study analyzed their ultrastructure using transmission electron microscopy. Putative Wolbachia cells were observed in the uninucleate bacteriocytes, which were packed with numerous Carsonella cells surrounded by host mitochondria, rough endoplasmic reticula, and the Golgi apparatus. Carsonella contained many ribosomes, parts of which formed conspicuous aggregates. The Carsonella envelope was lined with fiber bundles forming a net-like structure. In Profftella , numerous tubular structures were observed, each approximately 300 nm in diameter, consisting of several intertwined fibers. Some Profftella cells exhibited surface protrusions. The syncytium occasionally contained Profftella cells, apparently in the degradation process. Host organelles were less abundant in the syncytium than in the uninucleate bacteriocytes. Mitochondria in the syncytium had less developed cristae than those in the uninucleate bacteriocytes. These observations established a basis for understanding interactions among the host cells and bacterial symbionts. IMPORTANCE Omics analyses suggested a mutually indispensable tripartite association among the host D. citri and organelle-like bacteriome associates, Carsonella and Profftella , which are vertically transmitted through host generations. This relationship is based on the metabolic complementarity among these organisms, which is partly enabled by horizontal gene transfer between partners. However, little was known about the fine morphology of the symbionts and the bacteriome, the interface among these organisms. As a first step to address this issue, the present study performed transmission electron microscopy, which revealed previously unrecognized ultrastructures, including aggregations of ribosomes in Carsonella , numerous tubes and occasional protrusions of Profftella , apparently degrading Profftella , and host organelles with different abundance and morphology in distinct cell types. These findings provide insights into the behaviors of the symbionts and host cells to maintain the symbiotic relationship in D. citri.

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Section: Discussionsupporting

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Ultrastructure of the bacteriome and bacterial symbionts in the Asian citrus psyllid, Diaphorina citri

Nakabachi,

Suzaki

2024

Microbiol Spectr

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“…Plant-microbe interaction omics also helps us understand plant and microbial evolution and adaptation (Sa, 2024 ). Researchers can determine the genetics of trait variation, speciation events, and host-microbe co-evolutionary dynamics by comparing plant and microbe genomic and transcriptomic data across environments and evolutionary time scales (Kwak and Hansen, 2023 ; Mandal et al, 2023 ). These findings illuminate the evolutionary forces that shape biodiversity patterns and species interactions, informing conservation and ecosystem management strategies in the face of global environmental change.…”

Section: Omics Advancement and Applicationsmentioning

confidence: 99%

Omics approaches in understanding the benefits of plant-microbe interactions

Jain,

Sarsaiya,

Singh

et al. 2024

Front. Microbiol.

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Plant-microbe interactions are pivotal for ecosystem dynamics and sustainable agriculture, and are influenced by various factors, such as host characteristics, environmental conditions, and human activities. Omics technologies, including genomics, transcriptomics, proteomics, and metabolomics, have revolutionized our understanding of these interactions. Genomics elucidates key genes, transcriptomics reveals gene expression dynamics, proteomics identifies essential proteins, and metabolomics profiles small molecules, thereby offering a holistic perspective. This review synthesizes diverse microbial-plant interactions, showcasing the application of omics in understanding mechanisms, such as nitrogen fixation, systemic resistance induction, mycorrhizal association, and pathogen-host interactions. Despite the challenges of data integration and ethical considerations, omics approaches promise advancements in precision intervention and resilient agricultural practices. Future research should address data integration challenges, enhance omics technology resolution, explore epigenomics, and understand plant-microbe dynamics under diverse conditions. In conclusion, omics technologies hold immense promise for optimizing agricultural strategies and fortifying resilient plant-microbe alliances, paving the way for sustainable agriculture and environmental stewardship.

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A complete DNA repair system assembled by two endosymbionts restores heat tolerance of the insect host

Ling,

Guo,

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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DNA repair systems are essential to maintain genome integrity and stability. Some obligate endosymbionts that experience long-term symbiosis with the insect hosts, however, have lost their key components for DNA repair. It is largely unexplored how the bacterial endosymbionts cope with the increased demand for mismatch repairs under heat stresses. Here, we showed that ibpA, a small heat shock protein encoded by Buchnera aphidicola , directly interacted with the cytoskeletal actin to prevent its aggregation in bacteriocytes, thus reinforcing the stability of bacteriocytes. However, the succession of 11 adenines in the promoter of ibpA is extremely prone to mismatching error, e.g., a single adenine deletion, which impairs the induction of ibpA under heat stress. Coinfection with a facultative endosymbiont Serratia symbiotica remarkably reduced the mutagenesis rate in the Buchnera genome and potentially prevented a single adenine deletion in ibpA promoter, thereby alleviating the heat vulnerability of aphid bacteriocytes. Furthermore, Serratia encoded mutH, a conserved core protein of prokaryotic DNA mismatch repair (MMR), accessed to Buchnera cells, which complemented Buchnera mutL and mutS in constituting an active MMR. Our findings imply that a full complement of a prokaryotic MMR system assembled by two bacterial endosymbionts contributes significantly to the thermostability of aphid bacteriocytes in an ibpA-dependent manner, furnishing a distinct molecular link among tripartite symbioses in shaping resilience and adaptation of their insect hosts to occupy other ecological niches.

show abstract

Unveiling metabolic integration in psyllids and their nutritional endosymbionts through comparative transcriptomics analysis

Cited by 5 publications

References 92 publications

Ultrastructure of the bacteriome and bacterial symbionts in the Asian citrus psyllid, Diaphorina citri

Ultrastructure of the bacteriome and bacterial symbionts in the Asian citrus psyllid, Diaphorina citri

Omics approaches in understanding the benefits of plant-microbe interactions

A complete DNA repair system assembled by two endosymbionts restores heat tolerance of the insect host

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