Biology subjects

Stroinski, A.

Publications and source records attributed to Stroinski, A..

6 recordsLinked to original sources

bioRxiv2025

The tiniest genomes shrink much further: extreme reductive evolution in planthopper symbionts

Strictly heritable endosymbiotic bacteria that provide limiting nutrients to sap-sucking hemipteran insects are known for their highly reduced genomes conserved in organization and function. Here, we show how in ancestral endosymbionts of planthoppers, Sulcia and Vidania, gradually losing genes during [~]263 my of co-diversification with hosts, co-infections by additional microbes and host ecological switches coincided with more dramatic genomic changes. At its extremes, this has resulted in the smallest non-organellar bacterial genomes known, at barely 50-52 kb. Such minuscule Vidania genomes evolved convergently in two planthopper superfamilies, and are strikingly similar in gene contents, including the ability to produce a single amino acid (phenylalanine) for the host. Losing many additional cell-function genes places them among mitochondria in the level of host dependence, further blurring the bacteria-organelle boundary. One-sentence summaryWe present the smallest bacterial genomes known and evaluate the patterns and processes of their reductive evolution

evolutionary biology↗

bioRxiv2024

Phylogenomics resolves the relationship and the evolutionary history of planthoppers (Insecta: Hemiptera: Fulgoromorpha)

Planthoppers (Hemiptera: Fulgoromorpha) are a species-rich and globally distributed insect clade with high economic, ecological, and evolutionary importance. However, the relationships among planthopper lineages and families remain unclear. Previous efforts based on inconsistent morphological traits, a few genes, or limited sampling often resulted in conflicting tree topologies. Here, we used genome-level data to assemble 1164 nuclear single-copy genes and 13 mitochondrial protein-coding genes for 149 planthopper species representing 19 out of 21 extant families. Additional markers were added from published mitogenomes, expanding our sampling to 285 species. These markers were used for Maximum Likelihood-based tree inference and dating analyses. The newly inferred phylogenies validated well-accepted relationships and recovered novel placements. Taxonomic conclusions include the establishment of a new family Borysthenidae stat. rev. within Delphacoidea and a new superfamily Meenoploidea superfam. nov. including redefined Kinnaridae stat. rev. and Meenoplidae stat. rev., the confirmation of the monophyletic family Achilixiidae outside the Achilidae-Derbidae clade, and the transfer of tribes Lyncidini and Amyclini to Dictyopharidae and the genus Madagascaritia to Fulgoridae. The time analyses based on 57 nuclear markers and 30 fossils dated the origin of crown Fulgoromorpha back to Guadalupian, Permian ([~]263 Ma), close to the maximum constraint at 267.3 Ma, while applying an older root constraint resulted in an origin in Mississippian, Carboniferous ([~]332 Ma). While future sampling of unstudied fauna in unexplored regions or habitats may change the topology, the current phylogenomic analysis will serve as a solid foundation for research into planthopper ecology, evolution, and significance.

evolutionary biology↗

bioRxiv2023

Facultatively intra-bacterial localization of a planthopper endosymbiont as an adaptation to its vertical transmission

Transovarial transmission is the most reliable way of passing on essential nutrient- providing endosymbionts from mothers to offspring. However, not all endosymbiotic microbes follow the complex path through the female host tissues to oocytes on their own. Here we demonstrate an unusual transmission strategy adapted by one of the endosymbionts of the planthopper Trypetimorpha occidentalis (Hemiptera: Tropiduchidae) from Bulgaria. In this species, an Acetobacteraceae endosymbiont is transmitted transovarially within deep invaginations of cellular membranes of an ancient endosymbiont Sulcia - strikingly resembling recently described plant virus transmission. However, in males, Acetobacteraceae colonizes the same bacteriocytes as Sulcia but remains unenveloped. Then, the unusual endobacterial localization of Acetobacteraceae observed in females appears to be a unique adaptation to maternal transmission. Further, symbionts genomic features, including encoding essential amino acid biosynthetic pathways and very similar to a recently described psyllid symbiont, suggest a unique combination of ability to horizontally transmit among species and confer nutritional benefits. The close association with Acetobacteraceae symbiont correlates with the so-far- unreported level of genomic erosion of ancient nutritional symbionts of this planthopper. In Sulcia, this is reflected in substantial changes in genomic organization, reported for the first time in the symbiont renown for its genomic stability. In Vidania, substantial gene loss resulted in one of the smallest genomes known, at 109 kb. Thus, the symbionts of T. occidentalis display a combination of unusual adaptations and genomic features that expand our understanding of how insect-microbe symbioses may transmit and evolve. Significance StatementReliable transmission across host generations is a major challenge for bacteria that associate with insects, and independently established symbionts have addressed this challenge in different ways. The facultatively endobacterial association of Acetobacteraceae symbiont, enveloped by cells of ancient nutritional endosymbiont Sulcia in females but not males of the planthopper Trypetimorpha occidentalis, appears to be a unique adaptation to maternal transmission. Acetobacteraceaes genomic features indicate its unusual evolutionary history, and the genomic erosion experienced by ancient nutritional symbionts demonstrates apparent consequences of such close association. Combined, this multi-partite symbiosis expands our understanding of the diversity of strategies that insect symbioses form and some of their evolutionary consequences.

cell biology↗

bioRxiv2022

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

Sap-feeding hemipteran insects live in associations with diverse heritable endosymbiotic bacteria and fungi that provide essential nutrients deficient in their diets. These symbionts typically reside in bacteriomes, dedicated organs made up of specialized cells termed bacteriocytes. The bacteriome organization 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, 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 tissues and cell types, including bacteriocytes 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.

evolutionary biology↗

bioRxiv2022

Genome comparison reveals inversions and alternative evolutionary history of nutritional endosymbionts in planthoppers (Hemiptera: Fulgoromorpha)

The evolutionary success of sap-feeding hemipteran insects in the suborder Auchenorrhyncha was enabled by nutritional contributions from their heritable endosymbiotic bacteria. However, the symbiont diversity, functions, and evolutionary origins in this large insect group have not been broadly characterized using genomic tools. In particular, the origins and relationships among ancient betaproteobacterial symbionts Vidania (in Fulgoromorpha) and Nasuia/Zinderia (in Cicadomorpha) are uncertain. Here, we characterized the genomes of Vidania and Sulcia from three Pyrops planthoppers (family Fulgoridae) to understand their metabolic functions and evolutionary histories. Like in previously characterized planthoppers, these symbionts share nutritional responsibilities, with Vidania providing seven out of ten essential amino acids. Sulcia lineages across the Auchenorrhyncha have a highly conserved genome but with multiple independent rearrangements occurring in an early ancestor of Cicadomorpha or Fulgoromorpha and in a few succeeding lineages. Genomic synteny was also observed within each of the betaproteobacterial symbiont genera Nasuia, Zinderia, and Vidania, but not across them, which challenges the expectation of a shared ancestry for these symbionts. The further comparison of other biological traits strongly suggests an independent origin of Vidania early in the planthopper evolution and possibly of Nasuia and Zinderia in their respective host lineages. Originality-Significance StatementWe sequenced and characterized the genomes of two ancient nutritional symbionts, Sulcia and Vidania, in three species from the genus Pyrops in the species- and symbiont-rich but understudied insect clade, Fulgoromorpha (planthoppers). We describe--for the first time--several independent genome rearrangements in Sulcia, which is often cited as a premier example of extreme genome stability spanning hundreds of millions of years. We also show a global lack of synteny across the genomes of the Auchenorrhynchan betaproteobacterial symbionts (Vidania, Nasuia, and Zinderia). This result is unexpected given previous hypotheses of a common origin for these symbionts >250 million years ago alongside Sulcia. Taken together, we suggest an independent origin of Vidania and possibly of Nasuia and Zinderia symbiont lineages as well. This hypothesis further links the potential acquisition of novel nutritional endosymbiont lineages with the emergence of auchenorrhyncham superfamilies.

genomics↗

bioRxiv2021

Alternative transmission patterns in independently acquired nutritional co-symbionts of Dictyopharidae planthoppers

Sap-sucking hemipterans host specialized, heritable microorganisms that supplement their unbalanced diet with essential nutrients. These microbes show unusual features that provide a unique perspective on the evolution of life but have not been systematically studied. Here, we combine microscopy with high-throughput sequencing to revisit 80-year-old reports on the diversity of symbiont transmission modes in a broadly distributed planthopper family Dictyopharidae. We show that in all species examined, the ancestral nutritional endosymbionts Sulcia and Vidania are complemented by co-primary symbionts, either Arsenophonus or Sodalis, acquired several times independently by different host lineages. Like in other obligate sap-feeders, the ancestral symbionts produce essential amino acids, whereas co-primary symbionts contribute to the biosynthesis of B vitamins. These symbionts reside within separate bacteriomes within the abdominal cavity, although in females, Vidania also occupies bacteriocytes in the rectal organ. Notably, the symbionts are transmitted from mothers to offspring in two alternative ways. In most examined species, all nutritional symbionts simultaneously infect the posterior end of the full-grown (vitellogenic) oocytes and next gather in their perivitelline space. In contrast, in other species, Sodalis colonizes the cytoplasm of the anterior pole of young (previtellogenic) oocytes forming a cluster separate from the "symbiont ball" formed by late-invading Sulcia and Vidania. Our data add to evidence on frequent replacements of gammaproteobacterial symbionts combined with the relative functional stability of the nutritional functions during the evolution of sap-feeding insects, and show how newly-arriving microbes may utilize different strategies to establish long-term heritable symbiosis. Significance statementSup-sucking hemipterans host ancient heritable microorganisms that supplement their unbalanced diet with essential nutrients, and which have repeatedly been complemented or replaced by other microorganisms. They need to be reliably transmitted to subsequent generations through the reproductive system, and often they end up using the same route as the ancient symbionts. We show for the first time that in a single family of planthoppers, the complementing symbionts that have established infections independently utilize different transmission strategies, one of them novel, with the transmission of different microbes separated spatially and temporarily. These data show how newly-arriving microbes may utilize different strategies to establish long-term heritable symbiosis.

evolutionary biology↗