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We investigated the infection dynamics of endosymbiotic bacteria in the developmental course of the mealybugs Planococcus kraunhiae and Pseudococcus comstocki. Molecular phylogenetic analyses identified a betaproteobacterium and a gammaproteobacterium from each of the mealybug species.
The former bacterium was related to the β-endosymbionts of othe...
Citations
... T. princeps is regarded as the mealybug P-endosymbiont due to its widespread distribution and cocladogenesis with host insects (Munson et al. 1992). P -endosymbiont, T.princeps dominant in bacteriocytes specialized cells that are present in a structure called bacteriome within hemocoel of mealybugs (Kono et al. 2008) and can be transmitted vertically by hosts which are found in nearly all mealybug species that have a monophyletic origin (Downie and Gullan 2004;Baumann and Baumann 2005). Nonetheless, several P-endosymbionts belonging to the Bacteroidetes and β-proteobacteria groups have been discovered recently in the Phenacoccinae subfamily (Gruwell et al. 2010). ...
Hemiptera insects, like mealybug (Pseudococcidae family), pose a significant threat to agriculture, as evidenced by their status as a major pest and the existence of over 2,000 described species and 290 genera. Their destructive feeding habits lead to significant reductions in quality and productivity. In attempts to mitigate this problem, farmers often prefer the widespread use of synthetic insecticides. However, this conventional approach carries substantial drawbacks, like threats to human and environmental health, biomagnifications, the depletion of natural enemies, and resistance to target pests. The situation is more aggravated when water-based pesticides and biological control agents are quickly becoming ineffective by their cryptic lifestyle, hydrophobic wax covering, and the presence of gut endosymbionts of mealybugs, which together make their management difficult at best. The presence of symbiotic microbes in the saliva of phloem-sucking hemipterans, including mealybugs, enables these insect pests to defeat host plant defences and detoxify insecticides. Gut endosymbionts, wax-degrading bacteria, and entomopathogenic fungi are other promising eco-friendly agents that can channel to suppress populations of this polyphagous insect pest. Here, we review the analysis of conventional approaches to control mealybug infestations. Further, we explore eco-friendly alternatives and unravel cryptic interactions between mealybugs and associated microbes that would protect crops from the relentless menace of this assertive agricultural insect pest.
... Alongside closely related hemipterans such as aphids (Aphidomorpha) and whiteflies (Aleyrodomorpha) [30], scale insects (Coccomorpha) are sap-sucking and obligate plant parasites [31,32]. The feeding behavior of scale insects delays plant growth and, in severe infestations, can lead to the death of the entire plant [31]. ...
Insects possess an effective immune system, which has been extensively characterized in several model species, revealing a plethora of conserved genes involved in recognition, signaling, and responses to pathogens and parasites. However, some taxonomic groups, characterized by peculiar trophic niches, such as plant-sap feeders, which are often important pests of crops and forestry ecosystems, have been largely overlooked regarding their immune gene repertoire. Here we annotated the immune genes of soft scale insects (Hemiptera: Coccidae) for which omics data are publicly available. By using immune genes of aphids and Drosophila to query the genome of Ericerus pela, as well as the transcriptomes of Ceroplastes cirripediformis and Coccus sp., we highlight the lack of peptidoglycan recognition proteins, galectins, thaumatins, and antimicrobial peptides in Coccidae. This work contributes to expanding our knowledge about the evolutionary trajectories of immune genes and offers a list of promising candidates for developing new control strategies based on the suppression of pests’ immunity through RNAi technologies.
... PMB in their abdomen it carries a structure called bacteriome, that is packed with bacteriocytes whose cytoplasm is densely populated by endosymbiotic bacteria (Buchner, 1965). The mealybugs harbour a beta-proteobacterial maternally inherited primary endosymbiont, Tremblaya princeps and additional gammaproteobacterial secondary endosymbionts (Fukatsu and Nikoh 1998;von Dohlen et al. 2001;Thao et al. 2002;Kono et al., 2008;McCutcheon and von Dohlen 2011;Gatehouse et al., 2012). ...
... This resulted in the establishment of obligate co-diverging host-symbiont associations, accompanied by drastic reductions in the genome size of the symbiotic bacteria until only core housekeeping genes and biosynthetic pathways for the nutrients required by the insect hosts are retained [7][8][9] . Many sap-feeding hemipteran lineages, such as sternorrhynchans (aphids, adelgids, psyllids, scales, mealybugs) and auchenorrhynchans (planthoppers, spittlebugs, cicadas), are associated with more than one obligate endosymbiont [10][11][12][13][14][15][16][17][18][19][20][21][22][23] . In most dual endosymbiotic systems studied to date, the primary endosymbiont supplies the host with the majority of essential amino acids (EAAs), whereas the co-primary endosymbiont complements the genes or pathways that are no longer present in the primary endosymbiont [23][24][25][26][27][28][29] . ...
... Thus, the density of the aphid primary endosymbiont Buchnera increased throughout host ontogeny from embryos to young adults, indicating its important role during the different stages of insect development and reproduction, with a subsequent decrease of its titer during later stages of the aging host 34,38,45 . A similar pattern was found in obligate endosymbionts in several species of mealybugs across generations and life stages 11,18 . However, most studies were conducted under controlled environmental conditions and thus might display a much-reduced variation in the endosymbiont titers compared to natural populations, potentially due to the stabilization of the endosymbiont titer in a constant environment 18,46,47 . ...
Most sap-feeding insects maintain obligate relationships with endosymbiotic bacteria that provide their hosts with essential nutrients. However, knowledge about the dynamics of endosymbiont titers across seasons in natural host populations is scarce. Here, we used quantitative PCR to investigate the seasonal dynamics of the dual endosymbionts “ Candidatus Carsonella ruddii” and “ Ca. Psyllophila symbiotica” in a natural population of the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea: Psyllidae). Psyllid individuals were collected across an entire year, covering both summer and overwintering generations. Immatures harboured the highest titers of both endosymbionts, while the lowest endosymbiont density was observed in males. The density of Carsonella remained high and relatively stable across the vegetative period of the pear trees, but its density significantly dropped during the non-vegetative period, overlapping with C. pyricola ’s reproductive diapause. In contrast, the titer of Psyllophila was consistently higher than Carsonella ’s and exhibited fluctuations throughout the sampling year, which might be related to host age. Despite a tightly integrated metabolic complementarity between Carsonella and Psyllophila , our findings highlight differences in their density dynamics throughout the year, that might be linked to their metabolic roles at different life stages of the host.
... While Hodgkinia and Sulcia are spatially separated within the bacteriome, it is unlikely that Hodgkinia was excluded due to a dissection error (Van Leuven et al. 2014;Campbell et al. 2015;Łukasik et al. 2018). The lack of Hodgkinia material might instead suggest that this sample originated from a slightly older, senescent individual (Kono et al. 2008;Vigneron et al. 2014;Simonet et al. 2018). A sample from M. septendecim produced very little endosymbiont-derived RNA coverage in general, with Hodgkinia and Sulcia collectively contributing less than 0.1%, and was excluded from all other analysis (marked with two asterisks in fig. ...
Bacteria that form long-term intracellular associations with host cells lose many genes, a process that often results in tiny, gene-dense, and stable genomes. Paradoxically, the same evolutionary processes that drive genome reduction and simplification may sometimes cause genome expansion and complexification. A bacterial endosymbiont of cicadas, Hodgkinia cicadicola, exemplifies this paradox. In many cicada species, a single Hodgkinia lineage with a tiny, gene-dense genome has split into several interdependent cell and genome lineages. Each new Hodgkinia lineage encodes a unique subset of the ancestral unsplit genome in a complementary way, such that the collective gene contents of all lineages match the total found in the ancestral single genome. This splitting creates genetically distinct Hodgkinia cells that must function together to carry out basic cellular processes. It also creates a gene dosage problem where some genes are encoded by only a small fraction of cells while others are much more abundant. Here, by sequencing DNA and RNA of Hodgkinia from different cicada species with different amounts of splitting - along with its structurally stable, unsplit partner endosymbiont Sulcia muelleri - we show that Hodgkinia does not transcriptionally compensate to rescue the wildly unbalanced gene and genome ratios that result from lineage splitting. We also find that Hodgkinia has a reduced capacity for basic transcriptional control independent of the splitting process. Our findings reveal another layer of degeneration further pushing the limits of canonical molecular and cell biology in Hodgkinia and may partially explain its propensity to go extinct through symbiont replacement.
... KEYWORDS aphids, bacterial mutualism, bacteriocytes, co-obligate Serratia symbiotica, embryo invasion, gut symbiont I n many sap-feeding insects, bacterial mutualism for nutrition is based on the coexistence, within the same host, of multiple obligate bacteria that collectively function as a metabolic unit to produce nutrients that are lacking in the host's diet (1)(2)(3)(4)(5)(6)(7)(8). Previous observations indicate that the metabolic convergence of the bacterial cosymbionts composing these multisymbiotic systems goes hand in hand with the compartmentalization of those bacterial partners into symbiotic host cells (the bacteriocytes) that can be organized in a common symbiotic organ (the bacteriome) (1,(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16). In aphids (Hemiptera: Aphididae), nutritional disymbiotic systems have evolved on numerous occasions in species of the subfamilies Lachninae and Chaitophorinae (4,6,9,(17)(18)(19). ...
Multipartner nutritional endosymbioses have evolved many times in insects. In Chaitophorinae aphids, the eroded metabolic capabilities of the ancient obligate symbiont B. aphidicola are complemented by those of more recently acquired symbionts.
... El insecto D. texensis se alimenta de la savia de las plantas y provocan daños a las mismas por ser vectores de patógenos (Hardy et al., 2008;Kono et al., 2008;Vijay y Suresh, 2013). La extracción de savia se lleva a cabo por las ninfas y hembras adultas en su proceso de alimentación. ...
El objetivo del presente estudio fue desarrollar un método de control biológico eficaz para el manejo de Dysmicoccus texensis Tinsley en banano. Para ello, se determinó el mejor hospedero para la cría masiva de D. texensis, utilizando cinco ovisacos y 50 ninfas. El mejor hospedero fue el zapallo infestado con ovisacos, ya que obtuvo las mayores poblaciones del insecto. La preferencia del parasitoide al estado biológico de D. texensis se determinó utilizando el zapallo, infestado con 50 cochinillas del primer, segundo, tercer estadio y hembras adultas, mostrando una preferencia significativa por el segundo estadio ninfal. Se determinó la capacidad parasítica de Hambletonia pseudococcina Compere, parasitando entre 40 a 95 cochinillas durante su ciclo de vida. Se eligió el mejor alimento para el parasitoide utilizando dietas a base de agua, miel y polen, la dieta que contenía 1 mL agua + 4 mL miel + 0,01 mg de polen, alargó el tiempo de vida de los parasitoides. Al evaluar la eficacia en campo liberando 250 parejas de H. pseudococcina, se obtuvo el 62 % de parasitismo y una vez finalizada las liberaciones, se realizaron muestreos luego de tres meses, constatando la persistencia en campo con un 44 % de parasitismo.
... By high-temperature treatment and subsequent rearing on nutritionally rich whole wheat flour, a symbiont-free strain of O. surinamensis was established and maintained, and it continued to form atrophied sterile bacteriomes for 25 generations (67,68). In previous studies, histological observations of diverse insect-microbe symbiotic associations revealed that symbiont degeneration and/or loss tends to occur in a male-specific manner in aphids (61,(69)(70)(71), scale insects (72,73), lice (74,75), leaf beetles (15,23), powderpost beetles (30,76), and others (18), some of which also entail degeneration and/or loss of the symbiotic organs. Adult male insects do not grow, produce no eggs, and do not transmit the symbionts to the next generation, which plausibly account for the recurrent evolution of the male-specific symbiont losses. ...
Insects represent the biodiversity of the terrestrial ecosystem, and their prosperity is attributable to their association with symbiotic microorganisms. By sequestering microbial functionality into their bodies, organs, tissues, or cells, diverse insects have successfully exploited otherwise inaccessible ecological niches and resources, including herbivory enabled by utilization of indigestible plant cell wall components. In leaf beetles of the subfamily Cassininae, an ancient symbiont lineage, Stammera , whose genome is extremely reduced and specialized for encoding pectin-degrading enzymes, is hosted in gut-associated symbiotic organs and contributes to the host’s food plant digestion.
... Mealybugs ( Figure 1A) are insects that exclusively consume phloem sap and maintain nutritional endosymbiotic bacteria within specialized cells called bacteriocytes (Buchner, 1965;von Dohlen et al., 2001;Baumann et al., 2002). Mealybug bacteriocytes house between one and three different bacterial endosymbionts depending on the mealybug species (Kono et al., 2008;Koga et al., 2013;López-Madrigal et al., 2013;Husník and Mc-Cutcheon, 2016;Szabó et al., 2017;Gil et al., 2017). These mealybug endosymbionts produce essential amino acids and vitamins, which are present at low and variable levels in the insect's specialized plant sap diet. ...
Mealybugs are insects that maintain intracellular bacterial symbionts to supplement their nutrientpoor plant sap diets. Some mealybugs have a single betaproteobacterial endosymbiont, a Candidatus Tremblaya species (hereafter Tremblaya) that alone provides the insect with its required nutrients. Other mealybugs have two nutritional endosymbionts that together provide these nutrients, where Tremblaya has gained a gammaproteobacterial partner that resides in the cytoplasm of Tremblaya. Previous work had established that Pseudococcus longispinus mealybugs maintain not one but two species of gammaproteobacterial endosymbionts along with Tremblaya. Preliminary genomic analyses suggested that these two gammaproteobacterial endosymbionts have large genomes with features consistent with a relatively recent origin as insect endosymbionts, but the patterns of genomic complementarity between members of the symbiosis and their relative cellular locations were unknown. Here, using long-read sequencing and various types of microscopy, we show that the two gammaproteobacterial symbionts of P. longispinus are mixed together within Tremblaya cells, and that their genomes are somewhat reduced in size compared to their closest non-endosymbiotic relatives. Both gammaproteobacterial genomes contain thousands of pseudogenes, consistent with a relatively recent shift from a free-living to endosymbiotic lifestyle. Biosynthetic pathways of key metabolites are partitioned in complex interdependent patterns among the two gammaproteobacterial genomes, the Tremblaya genome, and horizontally acquired bacterial genes that are encoded on the mealybug nuclear genome. Although these two gammaproteobacterial endosymbionts have been acquired recently in evolutionary time, they have already evolved co-dependencies with each other, Tremblaya, and their insect host.
... Mealybugs ( Figure 1A) are insects that exclusively consume phloem sap and maintain nutritional endosymbiotic bacteria within specialized cells called bacteriocytes (Buchner, 1965;von Dohlen et al., 2001;Baumann et al., 2002). Mealybug bacteriocytes house between one and three different bacterial endosymbionts depending on the mealybug species (Kono et al., 2008;Koga et al., 2013;López-Madrigal et al., 2013;Husník and Mc-Cutcheon, 2016;Szabó et al., 2017;Gil et al., 2017). These mealybug endosymbionts produce essential amino acids and vitamins, which are present at low and variable levels in the insect's specialized plant sap diet. ...
Mealybugs are insects that maintain intracellular bacterial symbionts to supplement their nutrientpoor plant sap diets. Some mealybugs have a single betaproteobacterial endosymbiont, a Candidatus Tremblaya species (hereafter Tremblaya ) that alone provides the insect with its required nutrients. Other mealybugs have two nutritional endosymbionts that together provide these nutrients, where Tremblaya has gained a gammaproteobacterial partner that resides in the cytoplasm of Tremblaya . Previous work had established that Pseudococcus longispinus mealybugs maintain not one but two species of gammaproteobacterial endosymbionts along with Tremblaya . Preliminary genomic analyses suggested that these two gammaproteobacterial endosymbionts have large genomes with features consistent with a relatively recent origin as insect endosymbionts, but the patterns of genomic complementarity between members of the symbiosis and their relative cellular locations were unknown. Here, using long-read sequencing and various types of microscopy, we show that the two gammaproteobacterial symbionts of P. longispinus are mixed together within Tremblaya cells, and that their genomes are somewhat reduced in size compared to their closest non-endosymbiotic relatives. Both gammaproteobacterial genomes contain thousands of pseudogenes, consistent with a relatively recent shift from a free-living to endosymbiotic lifestyle. Biosynthetic pathways of key metabolites are partitioned in complex interdependent patterns among the two gammaproteobacterial genomes, the Tremblaya genome, and horizontally acquired bacterial genes that are encoded on the mealybug nuclear genome. Although these two gammaproteobacterial endosymbionts have been acquired recently in evolutionary time, they have already evolved co-dependencies with each other, Tremblaya , and their insect host.
Significance
Mealybugs are sap-feeding insects that house between one and three bacterial endosymbionts to supplement their nutritionally poor diets. Many mealybug-bacteria relationships were established tens or hundreds of millions of years ago, and these ancient examples show high levels host-endosymbiont genomic and metabolic integration. Here, we describe the complete genomes and cellular locations for two bacterial endosymbiont which have recently transitioned from a free-living to an intracellular state. Our work reveals the rapid emergence of metabolic interdependence between these two nascent endosymbionts, their partner bacterial co-symbiont in whose cytoplasm they reside, and their insect host cell. Our work confirms that intracellular bacteria rapidly adapt to a host-restricted lifestyle through breakage or loss of redundant genes.
