A Study on Symbiotic Systems of Cicadas Provides New Insights into Distribution of Microbial Symbionts and Improves Fluorescence In Situ Hybridization Technique

Huang, Zhi; Zhou, Jinrui; Zhang, Zhijun; He, Hong

doi:10.3390/ijms24032434

Cited by 9 publications

(5 citation statements)

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“…For example, gammaproteobacterial symbiont Arsenophonus usually occupies distinct bacteriomes. We found this type of organization in 7 out of 8 planthopper species harboring this symbiont, and it was previously reported from other hemipterans, including leafhoppers, cicadas, whiteflies, and scale insects ( Gottlieb et al, 2008 ; Kobiałka et al, 2018 ; Michalik et al, 2018b ; Huang et al, 2020 ; Huang et al, 2023 ). Other organization types are very unusual, and perhaps unique to planthoppers.…”

Section: Discussionsupporting

confidence: 86%

“…However, these symbioses are far from stable, with the relatively frequent acquisition of new microbes and symbiont replacement driving additional changes ( Sudakaran et al, 2017 ). Well-known examples of the replacement of an ancient symbiont include Sodalis instead of Zinderia in Philaenini spittlebugs ( Koga et al, 2013 ) and repeated replacements of Hodgkinia by Ophiocordyceps fungi in various lineages of cicadas ( Matsuura et al, 2018 ; Huang et al, 2020 ; Huang et al, 2023 ). Additional co-infecting microbes, especially Gammaproteobacteria related to Sodalis and Arsenophonus , have also been reported from many Auchenorrhyncha lineages and are typically linked to nutrition ( Michalik et al, 2021 )—although, in most cases, evidence is lacking, and the nature and stability of these associations unclear ( Michalik et al, 2014a ; Kobiałka et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

et al. 2023

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Sap-feeding hemipteran insects live in associations with diverse heritable symbiotic microorganisms (bacteria and fungi) that provide essential nutrients deficient in their hosts’ diets. These symbionts typically reside in highly specialized organs called bacteriomes (with bacterial symbionts) or mycetomes (with fungal symbionts). The organization of these organs varies between insect clades that are ancestrally associated with different microbes. As these symbioses evolve and additional microorganisms complement or replace the ancient associates, the organization of the symbiont-containing tissue becomes even more variable. Planthoppers (Hemiptera: Fulgoromorpha) are ancestrally associated with bacterial symbionts Sulcia and Vidania, but in many of the planthopper lineages, these symbionts are now accompanied or have been replaced by other heritable bacteria (e.g., Sodalis, Arsenophonus, Purcelliella) or fungi. We know the identity of many of these microbes, but the symbiont distribution within the host tissues and the bacteriome organization have not been systematically studied using modern microscopy techniques. Here, we combine light, fluorescence, and transmission electron microscopy with phylogenomic data to compare symbiont tissue distributions and the bacteriome organization across planthoppers representing 15 families. We identify and describe seven primary types of symbiont localization and seven types of the organization of the bacteriome. We show that Sulcia and Vidania, when present, usually occupy distinct bacteriomes distributed within the body cavity. The more recently acquired gammaproteobacterial and fungal symbionts generally occupy separate groups of cells organized into distinct bacteriomes or mycetomes, distinct from those with Sulcia and Vidania. They can also be localized in the cytoplasm of fat body cells. Alphaproteobacterial symbionts colonize a wider range of host body habitats: Asaia-like symbionts often colonize the host gut lumen, whereas Wolbachia and Rickettsia are usually scattered across insect tissues and cell types, including cells containing other symbionts, bacteriome sheath, fat body cells, gut epithelium, as well as hemolymph. However, there are exceptions, including Gammaproteobacteria that share bacteriome with Vidania, or Alphaproteobacteria that colonize Sulcia cells. We discuss how planthopper symbiont localization correlates with their acquisition and replacement patterns and the symbionts’ likely functions. We also discuss the evolutionary consequences, constraints, and significance of these findings.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

et al. 2023

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“…The fluorescence in situ hybridization (FISH) was conducted to reveal the distribution of symbionts in the fat bodies, bacteriomes and ovaries of different cicada species. The FISH assay was performed as previously described [ 25 , 58 , 59 ]. The probe and helper sequences used in this study were listed in Table S9.…”

Section: Methodsmentioning

confidence: 99%

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

Huang,

Wang,

Zhou

et al. 2024

Front Zool

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The most extraordinary systems of symbiosis in insects are found in the suborder Auchenorrhyncha of Hemiptera, which provide unique perspectives for uncovering complicated insect-microbe symbiosis. We investigated symbionts associated with bacteriomes and fat bodies in six cicada species, and compared transmitted cell number ratio of related symbionts in ovaries among species. We reveal that Sulcia and Hodgkinia or a yeast-like fungal symbiont (YLS) are segregated from other host tissues by the bacteriomes in the nymphal stage, then some of them may migrate to other organs (i.e., fat bodies and ovaries) during host development. Particularly, YLS resides together with Sulcia in the “symbiont ball” of each egg and the bacteriomes of young-instar nymphs, but finally migrates to the fat bodies of adults in the majority of Hodgkinia-free cicadas, whereas it resides in both bacteriome sheath and fat bodies of adults in a few other species. The transmitted Sulcia/YLS or Sulcia/Hodgkinia cell number ratio in ovaries varies significantly among species, which could be related to the distribution and/or lineage splitting of symbiont(s). Rickettsia localizes to the nuclei of bacteriomes and fat bodies in some species, but it was not observed to be transmitted to the ovaries, indicating that this symbiont may be acquired from environments or from father to offspring. The considerable difference in the transovarial transmission process of symbionts suggests that cellular mechanisms underlying the symbiont transmission are complex. Our results may provide novel insights into insect-microbe symbiosis.

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“…Commensal symbionts are microorganisms that live in close association with a host organism and benefit from this relationship without causing harm to the host 52 , 53 . For example, the gut microbiota is a complex and dynamic community of commensal bacteria, fungi, archaea, and viruses that colonize the gastrointestinal tract and influence various aspects of host physiology and immunity.…”

Section: Depleted Commensal Symbionts Negatively Regulate the Recruit...mentioning

confidence: 99%

A comprehensive perspective on the interaction between gut microbiota and COVID-19 vaccines

Hong

Lan

et al. 2023

Gut Microbes

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The efficacy of COVID-19 vaccines varies between individuals and populations, and the reasons for this are still not fully understood. Recent clinical studies and animal models have indicated that the gut microbiota may influence the immunogenicity of the vaccine and, thus, its effectiveness. This suggests that there is a bidirectional relationship between the gut microbiota and the COVID-19 vaccine, with the varying components of the microbiota either enhancing or reducing the vaccine’s efficacy. To put an end to the spread of the COVID-19 pandemic, the necessity of vaccines that create powerful and long-term immunity is now more important than ever, and understanding the role of the gut microbiota in this process is essential. Conversely, COVID-19 vaccines also have a significant effect on the gut microbiota, decreasing its total number of organisms and the variety of species present. In this Review, we analyze the evidence that suggesting an interaction between the gut microbiota and COVID-19 vaccine effectiveness, consider the immunological mechanisms that may be responsible for this connection, and explore the possibility of using gut microbiota-focused interventions to improve the efficacy of COVID-19 vaccines.

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A Study on Symbiotic Systems of Cicadas Provides New Insights into Distribution of Microbial Symbionts and Improves Fluorescence In Situ Hybridization Technique

Cited by 9 publications

References 53 publications

Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

A comprehensive perspective on the interaction between gut microbiota and COVID-19 vaccines

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