ABSTRACT
The genomes of obligate bacterial co-symbionts of the green rice leafhopper
Nephotettix cincticeps
, which is notorious as an agricultural pest, were determined. The streamlined genomes of “
Candidatus
Sulcia muelleri” and “
Candidatus
Nasuia deltocephalinicola” exhibited complementary metabolic pathways for synthesizing essential nutrients that contribute to host adaptation.
The genome of “
Candidatus
Regiella insecticola” strain TUt, a facultative bacterial symbiont of the pea aphid
Acyrthosiphon pisum
, was analyzed. We determined a 2.5-Mb draft genome consisting of 14 contigs; this will contribute to the understanding of the symbiont, which underpins various ecologically adaptive traits of the host insect.
“
Candidatus
Serratia symbiotica” is a facultative bacterial symbiont of aphids that affects various ecological traits of the host insects. Here, we report the complete genome sequence of “
Candidatus
Serratia symbiotica” strain IS, consisting of a 2,736,352-bp chromosome and an 82,605-bp plasmid, from the pea aphid
Acyrthosiphon pisum
.
ABSTRACT
Members of the genus
Rickettsiella
are bacterial pathogens of insects and other arthropods. Recently, a novel facultative endosymbiont, “
Candidatus
Rickettsiella viridis,” was described in the pea aphid
Acyrthosiphon pisum
, whose infection causes a striking host phenotype: red and green genetic color morphs exist in aphid populations, and upon infection with the symbiont, red aphids become green due to increased production of green polycyclic quinone pigments. Here we determined the complete genome sequence of the symbiont. The 1.6-Mb circular genome, harboring some 1,400 protein-coding genes, was similar to the genome of entomopathogenic
Rickettsiella grylli
(1.6 Mb) but was smaller than the genomes of phylogenetically allied human pathogens
Coxiella burnetii
(2.0 Mb) and
Legionella pneumophila
(3.4 Mb). The symbiont’s metabolic pathways exhibited little complementarity to those of the coexisting primary symbiont
Buchnera aphidicola
, reflecting the facultative nature of the symbiont. The symbiont genome harbored neither polyketide synthase genes nor the evolutionarily allied fatty acid synthase genes that are suspected to catalyze the polycyclic quinone synthesis, indicating that the green pigments are produced not by the symbiont but by the host aphid. The symbiont genome retained many type IV secretion system genes and presumable effector protein genes, whose homologues in
L. pneumophila
were reported to modulate a variety of the host's cellular processes for facilitating infection and virulence. These results suggest the possibility that the symbiont is involved in the green pigment production by affecting the host’s metabolism using the secretion machineries for delivering the effector molecules into the host cells.
IMPORTANCE
Insect body color is relevant to a variety of biological aspects such as species recognition, sexual selection, mimicry, aposematism, and crypsis. Hence, the bacterial endosymbiont “
Candidatus
Rickettsiella viridis,” which alters aphid body color from red to green, is of ecological interest, given that different predators preferentially exploit either red- or green-colored aphids. Here we determined the complete 1.6-Mb genome of the symbiont and uncovered that, although the red-green color transition was ascribed to upregulated production of green polycyclic quinone pigments, the symbiont genome harbored few genes involved in the polycyclic quinone biosynthesis. Meanwhile, the symbiont genome contained type IV secretion system genes and presumable effector protein genes, whose homologues modulate eukaryotic cellular processes for facilitating infection and virulence in the pathogen
Legionella pneumophila
. We propose the hypothesis that the symbiont may upregulate the host’s production of polycyclic quinone pigments via cooption of secretion machineries and effector molecules for pathogenicity.
ABSTRACT
Huanglongbing, or citrus greening, is a devastating disease of citrus plants recently spreading worldwide, which is caused by an uncultivable bacterial pathogen, “
Candidatus
Liberibacter asiaticus,” and vectored by a phloem-sucking insect,
Diaphorina citri
. We investigated the infection density dynamics of “
Ca
. Liberibacter asiaticus” in field populations of
D. citri
with experiments using field-collected insects to address how “
Ca
. Liberibacter asiaticus” infection density in the vector insect is relevant to pathogen transmission to citrus plants. Of 500 insects continuously collected from “
Ca
. Liberibacter asiaticus”-infected citrus trees with pathological symptoms in the spring and autumn of 2009, 497 (99.4%) were “
Ca
. Liberibacter asiaticus” positive. The infections were systemic across head-thorax and abdomen, ranging from 10
3
to 10
7
bacteria per insect. In spring, the infection densities were low in March, at ∼10
3
bacteria per insect, increasing up to 10
6
to 10
7
bacteria per insect in April and May, and decreasing to 10
5
to 10
6
bacteria per insect in late May, whereas the infection densities were constantly ∼10
6
to 10
7
bacteria per insect in autumn. Statistical analysis suggested that several factors, such as insect sex, host trees, and collection dates, may be correlated with “
Ca
. Liberibacter asiaticus” infection densities in field
D. citri
populations. Inoculation experiments with citrus seedlings using field-collected “
Ca
. Liberibacter asiaticus”-infected insects suggested that (i) “
Ca
. Liberibacter asiaticus”-transmitting insects tend to exhibit higher infection densities than do nontransmitting insects, (ii) a threshold level (∼10
6
bacteria per insect) of “
Ca
. Liberibacter asiaticus” density in
D. citri
is required for successful transmission to citrus plants, and (iii)
D. citri
attaining the threshold infection level transmits “
Ca
. Liberibacter asiaticus” to citrus plants in a stochastic manner. These findings provide valuable insights into understanding, predicting, and controlling this notorious citrus pathogen.
ABSTRACTA gammaproteobacterial facultative symbiont of the genusRickettsiellawas recently identified in the pea aphid,Acyrthosiphon pisum. Infection with this symbiont altered the color of the aphid body from red to green, potentially affecting the host's ecological characteristics, such as attractiveness to different natural enemies. In European populations ofA. pisum, the majority ofRickettsiella-infected aphids also harbor another facultative symbiont, of the genusHamiltonella. We investigated thisRickettsiellasymbiont for its interactions with the coinfectingHamiltonellasymbiont, its phenotypic effects onA. pisumwith and withoutHamiltonellacoinfection, and its infection prevalence inA. pisumpopulations. Histological analyses revealed that coinfectingRickettsiellaandHamiltonellaexhibited overlapping localizations in secondary bacteriocytes, sheath cells, and hemolymph, whileRickettsiella-specific localization was found in oenocytes.Rickettsiellainfections consistently altered hosts' body color from red to green, where the greenish hue was affected by both host and symbiont genotypes.Rickettsiella-Hamiltonellacoinfections also changed red aphids to green; this greenish hue tended to be enhanced byHamiltonellacoinfection. With different host genotypes,Rickettsiellainfection exhibited either weakly beneficial or nearly neutral effects on host fitness, whereasHamiltonellainfection andRickettsiella-Hamiltonellacoinfection had negative effects. Despite considerable frequencies ofRickettsiellainfection in European and North AmericanA. pisumpopulations, noRickettsiellainfection was detected among 1,093 insects collected from 14 sites in Japan. On the basis of these results, we discuss possible mechanisms for the interaction ofRickettsiellawith other facultative symbionts, their effects on their hosts' phenotypes, and their persistence in natural host populations. We propose the designation “CandidatusRickettsiella viridis” for the symbiont.
ABSTRACT
“
Candidatus
Midichloria mitochondrii” is an intramitochondrial bacterium of the order
Rickettsiales
associated with the sheep tick
Ixodes ricinus
. Bacteria phylogenetically related to “
Ca
. Midichloria mitochondrii” (midichloria and like organisms [MALOs]) have been shown to be associated with a wide range of hosts, from amoebae to a variety of animals, including humans. Despite numerous studies focused on specific members of the MALO group, no comprehensive phylogenetic and statistical analyses have so far been performed on the group as a whole. Here, we present a multidisciplinary investigation based on 16S rRNA gene sequences using both phylogenetic and statistical methods, thereby analyzing MALOs in the overall framework of the
Rickettsiales
. This study revealed that (i) MALOs form a monophyletic group; (ii) the MALO group is structured into distinct subgroups, verifying current genera as significant evolutionary units and identifying several subclades that could represent novel genera; (iii) the MALO group ranks at the level of described
Rickettsiales
families, leading to the proposal of the novel family “
Candidatus
Midichloriaceae.” In addition, based on the phylogenetic trees generated, we present an evolutionary scenario to interpret the distribution and life history transitions of these microorganisms associated with highly divergent eukaryotic hosts: we suggest that aquatic/environmental protista have acted as evolutionary reservoirs for members of this novel family, from which one or more lineages with the capacity of infecting metazoa have evolved.