Abstract
BackgroundObligate bacterial primary (P-) endosymbionts that are maternally inherited and codiverge with hosts are widespread across insect lineages with nutritionally restricted diets. Secondary (S-) endosymbionts are mostly facultative, but in some hosts, they complement P-endosymbiont function and therefore become obligate. Phylogenetic evidence exists for host switching and replacement of S-endosymbionts. The community dynamics that precede endosymbiont replacement and complementation have been little studied across host species, yet they are fundamental to the evolution of endosymbiosis.ResultsWe performed bacterial 16S rRNA gene amplicon sequencing of 25 psyllid species (Hemiptera, Psylloidea) across different developmental stages and ecological niches by focusing on the characterisation of the bacteria other than the universally present P-endosymbiont Carsonella (Gammaproteobacteria). Most species harboured only one dominant representative of diverse gammaproteobacterial S-endosymbionts that was consistently detected across all host individuals and populations (Arsenophonus in eight species, Sodalis or Sodalis-like bacteria in four species, unclassified Enterobacteriaceae in eight species). The identity of this dominant obligate S-endosymbiont varied across closely related host species. Unexpectedly, five psyllid species had two or three co-occurring endosymbiont species other than Carsonella within all host individuals, including a Rickettsiella-like bacterium (Gammaproteobacteria) in one psyllid species. Based on standard and quantitative PCR, all psyllids carried Carsonella, at higher titres than their dominant S-endosymbionts. Some psyllids also had Alphaproteobacteria (Lariskella, Rickettsia, Wolbachia) at varying prevalence. Incidence of other bacteria, including known plant pathogens, was low. Ecological niche of gall-forming, lerp-forming and free-living psyllid species did not impact endosymbiont communities. Two flush-feeding psyllid species had population-specific differences, and this was attributable to the higher endosymbiont diversity in native ranges and the absence of some endosymbionts in invasive ranges.ConclusionsOur data support the hypothesis of strict vertical transmission of minimal core communities of bacteria in psyllids. We also found evidence for S-endosymbiont replacement across closely related psyllid species. Multiple dominant S-endosymbionts present in some host species, including at low titre, constitute potential examples of incipient endosymbiont complementation or replacement. Our multiple comparisons of deep-sequenced minimal insect bacterial communities exposed the dynamics involved in shaping insect endosymbiosis.
Highlights
Obligate bacterial primary (P-) endosymbionts that are maternally inherited and codiverge with hosts are widespread across insect lineages with nutritionally restricted diets
Psyllid microbiota analysis using 16S rRNA gene amplicon sequencing A total of 191 individuals from 11 genera, comprising 20 taxa identified to species level and five taxa classified as two Glycaspis spp., two Creiis spp. and GB Cardiaspina sp., were subject to 16S rRNA gene amplicon sequencing and generated a total of 7,076,907 paired-end reads
For the remaining Operational taxonomic units (OTUs), seven chimeras were identified, but for six psyllid taxa, an excessive proportion of sequences were marked for removal by QIIME due to the identification of a single chimeric OTU common to most or all individuals in each species: for Aacanthocnema dobsoni, OTU56 constituting 39–99% of sequence reads obtained from all individual psyllids of this species; for Creiis sp., two OTU112 constituting 98.1–98.5%; for Pauropsylla depressa, OTU53 constituting 26–97%; for Eucalyptolyma maideni, OTU62 constituting 30.4–98.6%; and for Glycaspis sp., two OTU38 constituting 38.9–98.7%
Summary
Obligate bacterial primary (P-) endosymbionts that are maternally inherited and codiverge with hosts are widespread across insect lineages with nutritionally restricted diets. Insects that feed on plant sap or other nutritionally restricted diets depend on nutrient provisioning by primary (P-) endosymbionts that are localised within specialised host cells and omnipresent in host populations due to the efficient and strictly maternal endosymbiont transmission This results in co-evolution and can be seen in the phylogenetic congruency of bacterial endosymbionts and hosts [4]. Endosymbiosis drives the evolution of endosymbiont genomes towards accelerated mutation rates and the accumulation of non-lethal mutations [15], gene loss and sometimes lateral gene transfer to the host genome [16] This may necessitate complementation of P-endosymbiont function by facultative Sendosymbionts that can become obligate to hosts [3, 10]. A few studies have comprehensively characterised entire bacterial communities of hosts both within and across a significant number of species [9, 22], yet such studies are required to detect all present bacteria in hosts, including bacterial symbionts that may evolve from an indifferent transient role (as perhaps seen by a low prevalence or low bacterial titre) to a mutualistic role in their hosts (and they could be referred to as ‘symbionts in waiting’)
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