Ultrastructural and molecular characterization of endosymbionts of the reed beetle genusMacroplea(Chrysomelidae, Donaciinae), and proposal of “CandidatusMacropleicola appendiculatae” and “CandidatusMacropleicola muticae”

Kölsch, Gregor; Matz-Grund, Corinna Matz-GrundC.; Pedersen, Bo Vest

doi:10.1139/w09-085

Cited by 32 publications

(24 citation statements)

References 71 publications

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“…One obvious drawback of the current state is that many additional symbiotic lineages already known within Enterobacteriaceae cannot be at the moment included into serious phylogenetic analyses due to the lack of sufficient molecular data and will have to be revisited once complete genomic data are available. These bacteria include symbionts of mealybugs [ 89 , 102 ], psyllids [ 90 , 103 ], lice [ 2 , 91 ], weevils [ 11 , 12 , 92 ], reed beetles [ 104 , 105 ], true bugs [ 78 , 84 - 88 , 106 , 107 ] and symbionts of leeches [ 108 , 109 ]. Similarly, the importance of free-living bacteria and variety of S-symbionts as possible ancestors of P-symbionts should not be underestimated when assembling datasets for phylogenetic analyses.…”

Section: Discussionmentioning

confidence: 99%

Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches

2011

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BackgroundThe bacterial family Enterobacteriaceae gave rise to a variety of symbiotic forms, from the loosely associated commensals, often designated as secondary (S) symbionts, to obligate mutualists, called primary (P) symbionts. Determination of the evolutionary processes behind this phenomenon has long been hampered by the unreliability of phylogenetic reconstructions within this group of bacteria. The main reasons have been the absence of sufficient data, the highly derived nature of the symbiont genomes and lack of appropriate phylogenetic methods. Due to the extremely aberrant nature of their DNA, the symbiotic lineages within Enterobacteriaceae form long branches and tend to cluster as a monophyletic group. This state of phylogenetic uncertainty is now improving with an increasing number of complete bacterial genomes and development of new methods. In this study, we address the monophyly versus polyphyly of enterobacterial symbionts by exploring a multigene matrix within a complex phylogenetic framework.ResultsWe assembled the richest taxon sampling of Enterobacteriaceae to date (50 taxa, 69 orthologous genes with no missing data) and analyzed both nucleic and amino acid data sets using several probabilistic methods. We particularly focused on the long-branch attraction-reducing methods, such as a nucleotide and amino acid data recoding and exclusion (including our new approach and slow-fast analysis), taxa exclusion and usage of complex evolutionary models, such as nonhomogeneous model and models accounting for site-specific features of protein evolution (CAT and CAT+GTR). Our data strongly suggest independent origins of four symbiotic clusters; the first is formed by Hamiltonella and Regiella (S-symbionts) placed as a sister clade to Yersinia, the second comprises Arsenophonus and Riesia (S- and P-symbionts) as a sister clade to Proteus, the third Sodalis, Baumannia, Blochmannia and Wigglesworthia (S- and P-symbionts) as a sister or paraphyletic clade to the Pectobacterium and Dickeya clade and, finally, Buchnera species and Ishikawaella (P-symbionts) clustering with the Erwinia and Pantoea clade.ConclusionsThe results of this study confirm the efficiency of several artifact-reducing methods and strongly point towards the polyphyly of P-symbionts within Enterobacteriaceae. Interestingly, the model species of symbiotic bacteria research, Buchnera and Wigglesworthia, originated from closely related, but different, ancestors. The possible origins of intracellular symbiotic bacteria from gut-associated or pathogenic bacteria are suggested, as well as the role of facultative secondary symbionts as a source of bacteria that can gradually become obligate maternally transferred symbionts.

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Section: Discussionmentioning

confidence: 99%

Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches

2011

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“…Grain weevils (genus Sitophilus ) contain true endosymbionts that are transmitted through eggs and that live in cytosol of foregut cells of larvae and migrate to midgut epithelial cells in adults, apparently using bacterial type III secretion systems for cellular invasion (Dale et al ., ). The symbionts of reed beetles ( Chrysomelidae : Donaciinae) are also vertically transmitted but reside in the gut lumen; these associations resemble those of the plataspid– I. capsulata association described above (Kölsch et al ., ). The symbionts dominate the gut community and are concentrated in large midgut caecae in larvae and in specialized regions of Malpighian tubules in adults.…”

Section: Structure and Evolution Of Gut Microbial Communities In Insectsmentioning

confidence: 97%

The gut microbiota of insects – diversity in structure and function

2013

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Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.

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“…An additional factor to consider is that Hirsch et al (2012) used larvae hatched from surface-sterilized eggs for bacterial community characterization. Although bacterial transmission to progeny through the egg surface has not been studied in vine weevil, egg surface sterilization could potentially eliminate an important source of bacteria for the developing insect as has been described in other members of the Coleoptera order, such as the reed beetle genus Macroplea (K€ olsch et al, 2009;Kleinschmidt & K€ olsch, 2011) and the rove beetle Paederus sabaeus Erichson (Kellner, 2001(Kellner, , 2002. Therefore, to clarify the differences between the two studies, further research should aim to characterize bacterial microbiota of vine weevil larvae in comparison with egg and adult life stages.…”

Section: Discussionmentioning

confidence: 99%

The bacterial community associated with adult vine weevil (Otiorhynchus sulcatus) in UK populations growing on strawberry is dominated by Candidatus Nardonella

Morera‐Margarit

Bulgarelli

Pope

et al. 2019

Entomologia Exp Applicata

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Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), commonly known as black vine weevil or simply vine weevil, is an important pest of soft fruit and ornamental crops. This species is endemic to temperate areas of Europe but has spread to many other areas over the last century, including North America and Australasia. The ability of vine weevils to adapt to such different environments is difficult to reconcile with the parthenogenetic reproduction strategy, which is likely to underpin a low genetic diversity. It is therefore tempting to hypothesize that weevil adaptation to different environments is mediated, at least partly, by the microbial communities inhabiting these insects. As a first step towards testing this hypothesis we characterized the composition of the bacterial microbiota in weevils from populations feeding on strawberry plants across four geographically separate locations in the UK. We performed 16S rRNA gene Illumina amplicon sequencing, generating 2 882 853 high‐quality reads. Ecological indices, namely Chao1 and Shannon, revealed that the populations used for this study harboured a low diversity and an uneven bacterial microbiota. Furthermore, β‐diversity analysis failed to identify a clear association between microbiota composition and location. Notably, a single operational taxonomic unit phylogenetically related to Candidatus Nardonella accounted for 81% of the total sequencing reads for all tested insects. Our results indicate that vine weevil bacterial microbiota resembles that of other insects as it has low diversity and it is dominated by few taxa. A prediction of this observation is that location per se may not be a determinant of the microbiota inhabiting weevil populations. Rather, other or additional selective pressures, such as the plant species used as a food source, ultimately shape the weevil bacterial microbiota. Our results will serve as a reference framework to investigate other or additional hypotheses aimed at elucidating vine weevil adaptation to its environment.

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Ultrastructural and molecular characterization of endosymbionts of the reed beetle genusMacroplea(Chrysomelidae, Donaciinae), and proposal of “CandidatusMacropleicola appendiculatae” and “CandidatusMacropleicola muticae”

Cited by 32 publications

References 71 publications

Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches

Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches

The gut microbiota of insects – diversity in structure and function

The bacterial community associated with adult vine weevil (Otiorhynchus sulcatus) in UK populations growing on strawberry is dominated by Candidatus Nardonella

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