Publications

4851

Abstract Bacterial symbionts were shown to have significant beneficial impacts on the fitness of their host in insects, but little is known on the symbionts of spiders and their interactions with their hosts. Here, we assembled and investigated the circular 575 kb genome of Candidatus Argioplasma dusa, a novel bacterial symbiont of the wasp spider Argiope bruennichi . Phylogenomic analysis placed this species within the phylum Tenericutes, in a poorly characterized clade that may represent a new order-level lineage or affiliate with the Mycoplasmatales order. With 559 predicted genes, the genome is relatively small compared to other Tenericutes genomes (on average 969 genes) and has a low GC content of ~24%. While the genome encodes genes for proteins involved in glycolysis and fermentative acetate production, it revealed minimal biosynthetic capabilities with pathways for nucleotide, amino acid and vitamin biosynthesis being absent in Ca . Argioplasma dusa. This suggests an intracellular endosymbiotic lifestyle within the spider host. The symbiont was detected in A. bruennichi populations across the distribution range of the spider but appears to be absent in certain populations.

‘Candidatus Liberibacter asiaticus’ (CLas), the causal agent of citrus huanglongbing, is transmitted by the Asian citrus psyllid Diaphorina citri. While CLas-positive (CLas+) females exhibit increased fecundity and metabolic demands, their neuroendocrine regulation mechanisms remain unclear. We propose CLas manipulates dopamine (DA) signaling to enhance psyllid fecundity and CLas proliferation. Metabolomics revealed elevated DA in CLas+ females. Silencing DA synthesis genes and receptor DcDop2 via RNAi reduced lipid reserves, fecundity, and ovarian CLas titers. Through combined in vivo and in vitro experiments, we demonstrated that the microRNA miR-31a suppresses DcDop2 expression by binding to its 3’ untranslated region. Overexpression of miR-31a resulted in decreased DcDop2 expression and CLas titers in the ovaries, eliciting phenotypic defects akin to DcDop2 knockdown. Furthermore, DcDop2 knockdown and miR-31a overexpression reduced juvenile hormone (JH) levels and adipokinetic hormone (AKH) signaling in fat bodies and ovaries. Consequently, CLas regulates the DA-DcDop2 signaling axis to improve D. citri lipid metabolism and fecundity, while simultaneously promoting its replication. These findings reveal a coevolution between CLas proliferation and ovarian development in the insect host. This discovery enhances our understanding of the molecular interplay between plant pathogens and vector insects and offers novel targets and strategies for HLB field management.

Abstract De novo assembly of ancient and modern bacterial metagenomes can shed light on evolution and ecology of bacterial species that are challenging to culture. Tannerella and Porphyromonas are bacterial genera linked to periodontal disease, and understanding their evolution may reveal insights into their role in oral disease development. We performed pangenomic and phylogenetic analyses on a global set of isolates and metagenome-assembled genomes of the genera Tannerella (n = 238) and Porphyromonas (n = 976), including 66 genomes from ancient dental calculus samples (up to 14,800 years old), and modern oral samples from present-day living populations. We identify a novel species of oral Tannerella in modern and ancient humans, which we call Ca. Tannerella abscondita, that is related to and often mistaken for Tannerella forsythia but differs in its virulence repertoire. We reveal distinct niche tropism in Tannerella species and Porphyromonas pasteri, but not Porphyromonas gingivalis. There is limited phylogeographic structuring, and virulence genes are homogeneously distributed across continents and oral niches. Saliva-derived strains of T. forsythia and P. gingivalis from Oceania and T. serpentiformis and P. pasteri from Asia show enrichment of pseudogenes related to ecological niche transitions. A phylogenetic analysis of the P. gingivalis major fimbrial protein gene fimA reveals the genes cluster by genotypes, and that no ancient genes are found in genotypes I and Ib. Using de novo assembly for bacterial pangenomics improves the representation of oral genera found in reference databases and enhances our ability to study the evolutionary history of these taxa.