Extreme Polyploidy of
 Carsonella
 , an Organelle-Like Bacterium with a Drastically Reduced Genome

Nakabachi, Atsushi; Moran, Nancy A.

doi:10.1128/spectrum.00350-22

Cited by 18 publications

(24 citation statements)

References 27 publications

(48 reference statements)

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“…The D. citri hemocoel contains a symbiotic organ called the bacteriome ( 19 , 20 ), which harbors two distinct obligate mutualists, “ Candidatus Carsonella ruddii” ( Gammaproteobacteria : Oceanospirillales ) and “ Candidatus Profftella armatura” ( Gammaproteobacteria : Burkholderiales ) ( 21 , 22 ). “ Candidatus Carsonella” is a typical nutritional symbiont, providing its host with essential amino acids that are scarce in the phloem sap diet ( 21 , 23 , 24 ). In contrast, “ Candidatus Profftella” appears to be an organelle-like defensive symbiont, producing toxins that protect the holobiont (host plus symbionts) from natural enemies ( 21 , 25 ).…”

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confidence: 99%

Diaphorin, a Polyketide Produced by a Bacterial Symbiont of the Asian Citrus Psyllid, Inhibits the Growth and Cell Division of Bacillus subtilis but Promotes the Growth and Metabolic Activity of Escherichia coli

et al. 2022

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confidence: 99%

Diaphorin, a Polyketide Produced by a Bacterial Symbiont of the Asian Citrus Psyllid, Inhibits the Growth and Cell Division of Bacillus subtilis but Promotes the Growth and Metabolic Activity of Escherichia coli

et al. 2022

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“…Profftella armatura (Gammaproteobacteria: Burkholderiales) (21, 22). Carsonella is a typical nutritional symbiont, providing its host with essential amino acids that are scarce in the phloem sap diet (21, 23, 24). In contrast, Profftella appears to be an organelle-like defensive symbiont, producing toxins that protect the holobiont (host + symbionts) from natural enemies (21, 25).…”

Section: Introductionmentioning

confidence: 99%

Diaphorin, a polyketide produced by a bacterial symbiont of the Asian citrus psyllid, inhibits the growth of Bacillus subtilis but promotes the growth of Escherichia coli

Tanabe

Takasu

Hirose

et al. 2022

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Diaphorin is a polyketide produced by Candidatus Profftella armatura (Gammaproteobacteria: Burkholderiales), an obligate symbiont of a notorious agricultural pest, the Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae). Diaphorin belongs to the pederin family of bioactive agents found in various host-symbiont systems, including beetles, lichens, and sponges, harboring phylogenetically diverse bacterial producers. Previous studies showed that diaphorin has inhibitory effects on various eukaryotes, including the natural enemies of D. citri. However, little is known about its effects on prokaryotic organisms. To address this issue, the present study assessed the biological activities of diaphorin on two model prokaryotes, Escherichia coli (Gammaproteobacteria: Enterobacterales) and Bacillus subtilis (Firmicutes: Bacilli). The analyses revealed that diaphorin inhibits the growth of B. subtilis but moderately promotes the growth of E. coli. This finding implies that diaphorin functions as a defensive agent of the holobiont (host + symbionts) against some bacterial lineages but is beneficial for others, which potentially include obligate symbionts of D. citri.ImportanceCertain secondary metabolites, including antibiotics, evolve to mediate interactions among organisms. These molecules have distinct spectra for microorganisms and are often more effective against Gram-positive bacteria than Gram-negative ones. However, it is rare that a single molecule has completely opposite activities on distinct bacterial lineages. The present study revealed that a secondary metabolite synthesized by an organelle-like bacterial symbiont of psyllids inhibits the growth of Gram-positive Bacillus subtilis but promotes the growth of Gram-negative Escherichia coli. This finding not only provides insights into the evolution of symbiosis between animal hosts and bacteria but may also potentially be exploited to promote the effectiveness of industrial material production by microorganisms.

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“…“ Ca. Carsonella ruddii” ( Gammaproteobacteria : Oceanospirillales ) ( Thao et al , 2000b ; Spaulding and von Dohlen, 2001 ; Sloan and Moran, 2012 ; Nakabachi et al , 2013b , 2020a , 2020b , 2022 ; Arp et al , 2014 ; Hall et al , 2016 ; Morrow et al , 2017 ; Nakabachi and Moran, 2022 ) is the ‘primary symbiont’ that provides the host with essential amino acids ( Nakabachi et al , 2006 , 2013b , 2020b ; Sloan and Moran, 2012 ). Molecular phylogenetic analyses demonstrated cospeciation between psyllids and Carsonella , resulting from the single acquisition of a Carsonella ancestor by a psyllid common ancestor and its subsequent stable vertical transmission ( Thao et al , 2000b ; Spaulding and von Dohlen, 2001 ; Hall et al , 2016 ; Nakabachi et al , 2020a , 2022 ).…”

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High-resolution Microbiome Analyses of Nine Psyllid Species of the Family Triozidae Identified Previously Unrecognized but Major Bacterial Populations, including Liberibacter and Wolbachia of Supergroup O

2022

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Psyllids (Hemiptera: Sternorrhyncha: Psylloidea) are plant sap-sucking insects that include important agricultural pests. To obtain insights into the ecological and evolutionary behaviors of microbes, including plant pathogens, in Psylloidea, high-resolution analyses of the microbiomes of nine psyllid species belonging to the family Triozidae were performed using high-throughput amplicon sequencing of the 16S rRNA gene. Analyses identified various bacterial populations, showing that all nine psyllids have at least one secondary symbiont, along with the primary symbiont "Candidatus Carsonella ruddii" (Gammaproteobacteria: Oceanospirillales: Halomonadaceae). The majority of the secondary symbionts were gammaproteobacteria, particularly those of the order Enterobacterales, which included Arsenophonus and Serratia symbiotica, a bacterium formerly recognized only as a secondary symbiont of aphids (Hemiptera: Sternorrhyncha: Aphidoidea). The non-Enterobacterales gammaproteobacteria identified in the present study were Diplorickettsia (Diplorickettsiales: Diplorickettsiaceae), a potential human pathogen, and Carnimonas (Oceanospirillales: Halomonadaceae), a lineage detected for the first time in Psylloidea. Regarding alphaproteobacteria, the potential plant pathogen "Ca. Liberibacter europaeus" (Rhizobiales: Rhizobiaceae) was detected for the first time in Epitrioza yasumatsui, which feeds on the Japanese silverberry Elaeagnus umbellata (Elaeagnaceae), an aggressive invasive plant in the United States and Europe. Besides the detection of Wolbachia (Rickettsiales: Anaplasmataceae) of supergroup B in three psyllid species, a lineage belonging to supergroup O was identified for the first time in Psylloidea. These results suggest the rampant transfer of bacterial symbionts among animals and plants, thereby providing deeper insights into the evolution of interkingdom interactions among multicellular organisms and bacteria, which will facilitate the control of pest psyllids.

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Extreme Polyploidy of Carsonella , an Organelle-Like Bacterium with a Drastically Reduced Genome

Abstract: Mitochondria and plastids are endosymbiotic organelles in eukaryotic cells and are derived from free-living bacteria. They have many highly reduced genomes from which numerous genes have been transferred to the host nucleus.

Cited by 18 publications

References 27 publications

Diaphorin, a Polyketide Produced by a Bacterial Symbiont of the Asian Citrus Psyllid, Inhibits the Growth and Cell Division of Bacillus subtilis but Promotes the Growth and Metabolic Activity of Escherichia coli

Diaphorin, a Polyketide Produced by a Bacterial Symbiont of the Asian Citrus Psyllid, Inhibits the Growth and Cell Division of Bacillus subtilis but Promotes the Growth and Metabolic Activity of Escherichia coli

Diaphorin, a polyketide produced by a bacterial symbiont of the Asian citrus psyllid, inhibits the growth of Bacillus subtilis but promotes the growth of Escherichia coli

High-resolution Microbiome Analyses of Nine Psyllid Species of the Family Triozidae Identified Previously Unrecognized but Major Bacterial Populations, including <i>Liberibacter</i> and <i>Wolbachia</i> of Supergroup O

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