Biology subjects

McCutcheon, J. P.

Publications and source records attributed to McCutcheon, J. P..

7 recordsLinked to original sources

bioRxiv2026

A bacterial endosymbiont with a highly reduced genome forms extensive membrane contact sites with host organelles

Bacterial endosymbionts that establish long-term associations inside of host cells often lose a huge number of genes and become dependent on their hosts for essential cellular functions. One such example is the mealybug endosymbiont Tremblaya princeps: its ~139-kb genome encodes only ~120 protein coding genes and lacks all recognizable genes for lipid and fatty acid synthesis, cell wall components, membrane transport, protein translocation, and transmembrane proteins, raising fundamental questions of how Tremblaya's cellular envelope is formed and maintained. Here, using a combination of transmission electron microscopy (TEM) and focused ion beam scanning electron microscopy (FIB-SEM) of an entire endosymbiont-containing insect cell, we identified extensive and specific contacts between host cell mitochondria and Tremblaya. These contacts occurred at close membrane appositions and contained electron-dense bridge-like structures closely resembling classical eukaryotic membrane contact sites. Whole-cell segmentation showed that approximately 53% of host mitochondria were in contact with Tremblaya, with some mitochondria extensively wrapped by Tremblaya-associated membranes. Mitochondria in contact with Tremblaya were larger and contained proportionally greater cristae volume and surface density compared to non-contact mitochondria, exhibiting differences in both external and internal mitochondrial architecture. As membrane contact sites are well known to mediate lipid and metabolite exchange between membranes, these findings suggest that direct interactions with host organelles may be a source of vital membrane and cellular components for endosymbionts that have lost the autonomous ability to produce and transport these molecules.

microbiology↗

bioRxiv2024

Paternal genome elimination creates contrasting evolutionary trajectories in male and female citrus mealybugs

Most studies of sex-biased genes explore their evolution in familiar chromosomal sex determination systems, leaving the evolution of sex differences under alternative reproductive systems unknown. Here we explore the system of paternal genome elimination employed by mealybugs (Hempitera: Pseudococcidae) which have no sex chromosomes. Instead, all chromosomes are autosomal and inherited in two copies, but sex is determined by the ploidy of expression. Females express both parental alleles, but males reliably silence their paternally inherited chromosomes, creating genome-wide haploid expression in males and diploid expression in females. Additionally, sons do not express alleles directly inherited from their fathers, potentially disrupting the evolution of male-benefitting traits. To understand how these dynamics impact molecular evolution, we generated sex-specific RNAseq, a new gene annotation, and whole-genome population sequencing of the citrus mealybug, Planococcus citri. We found that genes expressed primarily in females hold more variation and evolve more quickly than those expressed in males or both sexes. Conversely, more adaptation occurs in genes expressed mainly in males than those expressed in females. Put together, paternal genome elimination appears to slow change on the male side but, by increasing selective scrutiny, increase the amount of adaptation in these genes. These results expand our understanding of evolution in a non-mendelian genetic system and the data we generated should prove useful for future research on this pest insect.

evolutionary biology↗

bioRxiv2024

Retention of an endosymbiont for the production of a single molecule

Sap-feeding insects often maintain multiple nutritional endosymbionts, which act in concert to produce compounds essential for insect survival. Many mealybugs have endosymbionts in a nested configuration: one or two bacterial species reside within the cytoplasm of another bacterium, and to-gether these bacteria have genomes which encode interdependent but complete sets of genes needed to produce key nutritional molecules. Here we show that the mealybug Pseudococcus viburni has three endosymbionts, one of which contributes only two genes that produce a single host nutrition-related molecule. All three bacterial endosymbionts have tiny genomes, suggesting that they have been co-evolving inside their insect host for millions of years. SignificanceNutritional endosymbionts synthesize (or contribute to the synthesis of) key metabolites such as essential amino acids and vitamins for their host organism. These nutrients are required by hosts because of their restricted diets, which in the case of mealybugs consists solely of plant phloem sap. Genome sequencing of insect endosymbionts has shown that their genomes can be very small, encoding few genes outside of core bacterial processes and nutrient provisioning. Here we highlight an example that has taken this reductive process to the extreme: a mealybug endosymbiont contributes only a single essential compound, chorismate, to the symbiosis.

evolutionary biology↗

bioRxiv2021

Host-associated microbial diversity in New Zealand cicadas uncovers elevational structure and replacement of obligate bacterial endosymbionts by Ophiocordyceps fungal pathogens

Host-microbe interactions influence eukaryotic evolution, particularly in the sap-sucking insects that often rely on obligate microbial symbionts to provision deficient nutrients in their diets. Cicadas (Hemiptera: Auchenorrhyncha: Cicadidae) specialize on xylem fluid and derive many essential amino acids and vitamins from intracellular bacteria or fungi (Hodgkinia, Sulcia, and Ophiocordyceps) that are propagated via transmission from mothers to offspring. Despite the beneficial role of these symbionts in nutrient provisioning, they are generally not considered to function within the gut where microbiota may play an important dietary role during insect diversification. Here, we investigate the relative impact of host phylogeny and ecology on gut microbial diversity in cicadas by sequencing 16S ribosomal RNA gene amplicons from 197 wild-collected cicadas and new mitochondrial genomes across 38 New Zealand cicada species, including natural hybrids between one species pair. We find a lack of phylogenetic structure and hybrid effects but a significant role of elevation in explaining variation in gut microbiota. Additionally, we provide evidence of Hodgkinia loss with gains of Ophiocordyceps fungal pathogens in all New Zealand cicadas examined that suggests convergent domestications of fungal pathogens. This highlights the macroevolutionary instability of obligate symbiosis and the relative importance of ecology rather than phylogeny for structuring gut microbial diversity in cicadas. ImportanceAn unresolved question in evolutionary biology is how beneficial associations between eukaryotes and microbes impact macroevolutionary patterns. We report substantial data from natural populations that suggest the absence of macroevolutionary impacts from gut microbiota in cicadas. Instead, gut microbial diversity is better explained by elevational variation across an island landscape. Cicadas, like many insects, have obligate nutritional associations with bacteria housed in organs outside of the gut, but we show that these associations seem also to be unstable at macroevolutionary scales. We report evidence for unexpected and widespread replacement of obligate bacteria by a domesticated and formerly pathogenic Ophiocordyceps fungus representing an evolutionarily convergent pattern across the cicada phylogeny.

evolutionary biology↗

bioRxiv2021

The evolution of interdependence in a four-way mealybug symbiosis

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. SignificanceMealybugs 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.

evolutionary biology↗

bioRxiv2018

Changes in endosymbiont complexity drive host-level compensatory adaptations in cicadas

For insects that depend on one or more bacterial endosymbionts for survival, it is critical that these bacteria are faithfully transmitted between insect generations. Cicadas harbor two essential bacterial endosymbionts, Sulcia muelleri and Hodgkinia cicadicola. In some cicada species, Hodgkinia has fragmented into multiple distinct cellular and genomic lineages that can differ in abundance by more than two orders of magnitude. This complexity presents a potential problem for the host cicada, because low-abundance-but-essential Hodgkinia lineages risk being lost during the symbiont transmission bottleneck from mother to egg. Here we show that all cicada eggs seem to receive the full complement of Hodgkinia lineages, and that in cicadas with more complex Hodgkinia this outcome is achieved by increasing the number of Hodgkinia cells transmitted by up to six-fold. We further show that cicada species with varying Hodgkinia complexity do not visibly alter their transmission mechanism at the resolution of cell biological structures. Together these data suggest that a major cicada adaptation to changes in endosymbiont complexity is an increase in the number of Hodgkinia cells transmitted to each egg. We hypothesize that the requirement to increase the symbiont titer is one of the costs associated with Hodgkinia fragmentation.

evolutionary biology↗

bioRxiv2017

Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas

When a free-living bacterium transitions to a host-beneficial endosymbiotic lifestyle, it almost invariably loses a large fraction of its genome [1, 2]. The resulting small genomes often become unusually stable in size, structure, and coding capacity [3-5]. Candidatus Hodgkinia cicadicola (Hodgkinia), a bacterial endosymbiont of cicadas, sometimes exemplifies this genomic stability. The Hodgkinia genome has remained completely co-linear in some cicadas diverged by tens of millions of years [6, 7]. But in the long-lived periodical cicada Magicicada tredecim, the Hodgkinia genome has split into dozens of tiny, gene-sparse genomic circles that sometimes reside in distinct Hodgkinia cells [8]. Previous data suggested that other Magicicada species harbor similarly complex Hodgkinia populations, but the timing, number of origins, and outcomes of the splitting process were unknown. Here, by sequencing Hodgkinia metagenomes from the remaining six Magicicada species and two sister species, we show that all Magicicada species harbor Hodgkinia populations of at least twenty genomic circles each. We find little synteny among the 256 Hodgkinia circles analyzed except between the most closely related species. Individual gene phylogenies show that Hodgkinia first split in the common ancestor of Magicicada and its closest known relatives, but that most splitting has occurred within Magicicada and has given rise to highly variable Hodgkinia gene dosages between cicada species. These data show that Hodgkinia genome degradation has proceeded down different paths in different Magicicada species, and support a model of genomic degradation that is stochastic in outcome and likely nonadaptive for the host. These patterns mirror the genomic instability seen in some mitochondria.

evolutionary biology↗