scholarly journals A Freeloader?: The Highly Eroded Yet large Genome of the Serratia symbiotica symbiont of Cinara strobi

2018 ◽  
Author(s):  
Alejandro Manzano-Marín ◽  
Armelle Coeur d’acier ◽  
Anne-Laure Clamens ◽  
Céline Orvain ◽  
Corinne Cruaud ◽  
...  
Keyword(s):  
Amplicon Sequencing ◽  
Genome Reduction ◽  
The Novel ◽  
Bacterial Symbionts ◽  
Buchnera Aphidicola ◽  
Essential Nutrients ◽  
Apparent Lack ◽  
Obligate Symbiont ◽  
Bacterial Endosymbionts ◽  
Serratia Symbiotica

ABSTRACTGenome reduction is pervasive among maternally-inherited bacterial endosymbionts. This genome reduction can eventually lead to serious deterioration of essential metabolic pathways, thus rendering an obligate endosymbiont unable to provide essential nutrients to its host. This loss of essential pathways can lead to either symbiont complementation (sharing of the nutrient production with a novel co-obligate symbiont) or symbiont replacement (complete takeover of nutrient production by the novel symbiont). However, the process by which these two evolutionary events happen remains somewhat enigmatic by the lack of examples of intermediate stages of this process. Cinara aphids (Hemiptera: Aphididae) typically harbour two obligate bacterial symbionts: Buchnera and Serratia symbiotica. However, the latter has been replaced by different bacterial taxa in specific lineages, and thus species within this aphid lineage could provide important clues into the process of symbiont replacement. In the present study, using 16S rRNA high-throughput amplicon sequencing, we determined that the aphid Cinara strobi harbours not two, but three fixed bacterial symbionts: Buchnera aphidicola, a Sodalis sp., and S. symbiotica. Through genome assembly and genome-based metabolic inference, we have found that only the first two symbionts (Buchnera and Sodalis) actually contribute to the hosts’ supply of essential nutrients while S. symbiotica has become unable to contribute towards this task. We found that S. symbiotica has a rather large and highly eroded genome which codes only for a few proteins and displays extensive pseudogenisation. Thus, we propose an ongoing symbiont replacement within C. strobi, in which a once ‘‘competent” S. symbiotica does no longer contribute towards the beneficial association. These results suggest that in dual symbiotic systems, when a substitute co-symbiont is available, genome deterioration can precede genome reduction and a symbiont can be maintained despite the apparent lack of benefit to its host.

scholarly journals Sequence of a Coxiella endosymbiont of the tick Amblyomma nuttalli suggests a pattern of convergent genome reduction in the Coxiella genus

2020 ◽  
Author(s):  
Tiago Nardi ◽  
Emanuela Olivieri ◽  
Edward Kariuki ◽  
Davide Sassera ◽  
Michele Castelli
Keyword(s):  
Coxiella Burnetii ◽  
Phylogenetic Analyses ◽  
Genome Reduction ◽  
Metabolic Profiles ◽  
The Novel ◽  
Bacterial Symbionts ◽  
Human Pathogen ◽  
Host Genus ◽  
Supportive Role ◽  
Genus One

Abstract Ticks require bacterial symbionts for the provision of necessary compounds that are absent in their hematophagous diet. Such symbionts are frequently vertically transmitted and, most commonly, belong to the Coxiella genus, which also includes the human pathogen Coxiella burnetii. This genus can be divided in four main clades, presenting partial but incomplete co-cladogenesis with the tick hosts. Here we report the genome sequence of a novel Coxiella, endosymbiont of the African tick Amblyomma nuttalli, and the ensuing comparative analyses. Its size (~1 Mb) is intermediate between symbionts of Rhipicephalus species and other Amblyomma species. Phylogenetic analyses show that the novel sequence is the first genome of the B clade, the only one for which no genomes were previously available. Accordingly, it allows to draw an enhanced scenario of the evolution of the genus, one of parallel genome reduction of different endosymbiont lineages, which are now at different stages of reduction from a more versatile ancestor. Gene content comparison allows to infer that the ancestor could be reminiscent of Coxiella burnetii. Interestingly, the convergent loss of mismatch repair could have been a major driver of such reductive evolution. Predicted metabolic profiles are rather homogenous among Coxiella endosymbionts, in particular vitamin biosynthesis, consistently with a host-supportive role. Concurrently, similarities among Coxiella endosymbionts according to host genus and despite phylogenetic unrelatedness hint at possible host-dependent effects.

scholarly journals Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

2019 ◽  
Vol 14 (1) ◽  
pp. 259-273 ◽  
Author(s):  
Alejandro Manzano-Marı́n ◽  
Armelle Coeur d’acier ◽  
Anne-Laure Clamens ◽  
Céline Orvain ◽  
Corinne Cruaud ◽  
...  
Keyword(s):  
In Situ Hybridisation ◽  
Essential Amino Acids ◽  
Aphid Species ◽  
Fluorescence In Situ Hybridisation ◽  
The Novel ◽  
Buchnera Aphidicola ◽  
Biosynthetic Genes ◽  
Obligate Symbiont

Abstract Many insects depend on obligate mutualistic bacteria to provide essential nutrients lacking from their diet. Most aphids, whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera aphidicola to supply essential amino acids and B vitamins. However, in some aphid species, provision of these nutrients is partitioned between Buchnera and a younger bacterial partner, whose identity varies across aphid lineages. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. It is also unclear whether the novel symbionts merely compensate for losses in Buchnera or carry new nutritional functions. Using whole-genome endosymbiont sequences of nine Cinara aphids that harbour an Erwinia-related symbiont to complement Buchnera, we show that the Erwinia association arose from a single event of symbiont lifestyle shift, from a free-living to an obligate intracellular one. This event resulted in drastic genome reduction, long-term genome stasis, and co-divergence with aphids. Fluorescence in situ hybridisation reveals that Erwinia inhabits its own bacteriocytes near Buchnera’s. Altogether these results depict a scenario for the establishment of Erwinia as an obligate symbiont that mirrors Buchnera’s. Additionally, we found that the Erwinia vitamin-biosynthetic genes not only compensate for Buchnera’s deficiencies, but also provide a new nutritional function; whose genes have been horizontally acquired from a Sodalis-related bacterium. A subset of these genes have been subsequently transferred to a new Hamiltonella co-obligate symbiont in one specific Cinara lineage. These results show that the establishment and dynamics of multi-partner endosymbioses can be mediated by lateral gene transfers between co-ocurring symbionts.

scholarly journals A genome-scale study of metabolic complementation in endosymbiotic consortia: the case of the cedar aphid

2017 ◽  
Author(s):  
Miguel Ponce-de-Leon ◽  
Daniel Tamarit ◽  
Jorge Calle-Espinosa ◽  
Matteo Mori ◽  
Amparo Latorre ◽  
...  
Keyword(s):  
Essential Amino Acids ◽  
Bacterial Consortium ◽  
Buchnera Aphidicola ◽  
Knock Out ◽  
A Genome ◽  
Complete Networks ◽  
Small Set ◽  
Bacterial Endosymbionts ◽  
Serratia Symbiotica ◽  
Genome Scale

AbstractBacterial endosymbionts and their insect hosts establish an intimate metabolic relationship. Bacteria offer a variety of essential nutrients to their hosts, whereas insect cells provide the necessary sources of matter and energy to their tiny metabolic allies. These nutritional complementations sustain themselves on a diversity of metabolite exchanges between the cell host and the reduced yet highly specialized bacterial metabolism –which, for instance, overproduces a small set of essential amino acids and vitamins. A well-known case of metabolic complementation is provided by the cedar aphid Cinara cedri that harbors two co-primary endosymbionts, Buchnera aphidicola BCc and Ca. Serratia symbiotica SCc, and in which some metabolic pathways are partitioned between different partners. Here we present a genome scale metabolic network (GEM) for the bacterial consortium from the cedar aphid iBSCc. The analysis of this GEM allows us the confirmation of cases of metabolic complementation previously described by genome analysis (i.e. tryptophan and biotin biosynthesis) and the proposal of a hitherto unnoticed event of metabolic pathway sharing between the two endosymbionts, namely the biosynthesis of tetrahydrofolate. In silico knock-out experiments with iBSCc showed that the consortium metabolism is a highly integrated yet fragile network. We also have explored the evolutionary pathways leading to the emergence of metabolic complementation between reduced metabolisms starting from individual, complete networks. Our results suggest that, during the establishment of metabolic complementation in endosymbionts, adaptive evolution is more significant than previously thought.

scholarly journals Role of Host Nutrition in Symbiont Regulation: Impact of Dietary Nitrogen on Proliferation of Obligate and Facultative Bacterial Endosymbionts of the Pea Aphid Acyrthosiphon pisum

2006 ◽  
Vol 73 (4) ◽  
pp. 1362-1366 ◽  
Author(s):  
T. L. Wilkinson ◽  
R. Koga ◽  
T. Fukatsu
Keyword(s):  
Population Density ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Buchnera Aphidicola ◽  
Nitrogen Levels ◽  
Dietary Nitrogen ◽  
Obligate Symbiont ◽  
Host Nutrition ◽  
Bacterial Endosymbionts ◽  
The Impact

ABSTRACT The impact of host nutrition on symbiont regulation in the pea aphid Acyrthosiphon pisum was investigated. The population density of the obligate symbiont Buchnera aphidicola positively correlated with dietary nitrogen levels. In contrast, the population density of the facultative symbiont Serratia symbiotica increased in aphids reared on low-nitrogen diets, indicating distinct regulatory mechanisms in the same insect host.

scholarly journals Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

2020 ◽  
Author(s):  
Shifen Xu ◽  
Liyun Jiang ◽  
Gexia Qiao ◽  
Jing Chen
Keyword(s):  
Myzus Persicae ◽  
Host Plants ◽  
Statistical Tests ◽  
Amplicon Sequencing ◽  
Symbiotic Bacteria ◽  
Bacterial Symbionts ◽  
Buchnera Aphidicola ◽  
Polyphagous Insects ◽  
First Time ◽  
Aphid Populations

Abstract Aphids are known to be associated with a variety of symbiotic bacteria. To improve our knowledge of the bacterial diversity of polyphagous aphids, in the present study, we investigated the microbiota of the cosmopolitan agricultural pest Myzus persicae (Sulzer). Ninety-two aphid samples collected from different host plants in various regions of China were examined using high-throughput amplicon sequencing. We comprehensively characterized the symbiont diversity of M. persicae and assessed the variations in aphid-associated symbiont communities. We detected a higher diversity of symbionts than has been previously observed. M. persicae hosted the primary endosymbiont Buchnera aphidicola and seven secondary symbionts, among which Wolbachia was the most prevalent and Rickettsia, Arsenophonus, and Spiroplasma were reported for the first time. Ordination analyses and statistical tests revealed that the symbiont flora associated with M. persicae did not change with respect to host plant or geography, which may be due to frequent migrations between different aphid populations. These findings will advance our knowledge of the microbiota of polyphagous insects and will enrich our understanding of assembly of host-microbiome systems.

scholarly journals Parallel evolution in the integration of a co-obligate aphid symbiosis

2020 ◽  
Author(s):  
David Monnin ◽  
Raphaella Jackson ◽  
E. Toby Kiers ◽  
Marie Bunker ◽  
Jacintha Ellers ◽  
...  
Keyword(s):  
Essential Amino Acid ◽  
Parallel Evolution ◽  
Buchnera Aphidicola ◽  
Energetic Costs ◽  
Sequence Of Events ◽  
Obligate Symbiont ◽  
Sap Feeding ◽  
Serratia Symbiotica ◽  
Nutrient Provisioning ◽  
Metabolic Unit

SUMMARYInsects evolve dependencies - often extreme - on microbes for nutrition. These include cases where insects harbour multiple endosymbionts that function collectively as a metabolic unit. How do these metabolic co-dependencies originate, and is there a predictable sequence of events leading to the integration of new symbionts? While dependency on multiple nutrient-provisioning symbionts has evolved numerous times across sap-feeding insects, there is only one known case of metabolic co-dependency in aphids, between Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily. Here we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. A comparison of recent and ancient associations allows us to investigate intermediate stages of metabolic and physical integration between the typically facultative symbiont, Serratia, and the ancient obligate symbiont Buchnera. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner, through parallel evolutionary processes. Specifically, we show (i) how the repeated losses of the riboflavin pathway in Buchnera leads to dependency on Serratia, (ii) evidence of a stepwise process of symbiont integration, whereby dependency evolves first, then essential amino acid pathways are lost (at ~30-60MYA), which coincides with increased physical integration of the companion symbiont; and (iii) dependency can evolve prior to specialised structures (e.g. bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesising nutrients may provide a unified explanation for the sequence of gene loses that occur during the evolution of co-obligate symbiosis.

scholarly journals Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome

EvoDevo ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Celeste R. Banfill ◽  
Alex C. C. Wilson ◽  
Hsiao-ling Lu
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Acyrthosiphon Pisum ◽  
Essential Amino Acids ◽  
Developmental Time ◽  
Follicular Epithelium ◽  
Future Research ◽  
Buchnera Aphidicola ◽  
Bacterial Endosymbionts ◽  
Asexual Embryogenesis

Abstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that provide essential nutrients. To advance understanding of the developmental and metabolic integration of hosts and endosymbionts, we track the localization of a non-essential amino acid transporter, ApNEAAT1, across asexual embryogenesis in the aphid, Acyrthosiphon pisum. Previous work in adult bacteriomes revealed that ApNEAAT1 functions to exchange non-essential amino acids at the A. pisum/Buchnera aphidicola symbiotic interface. Driven by amino acid concentration gradients, ApNEAAT1 moves proline, serine, and alanine from A. pisum to Buchnera and cysteine from Buchnera to A. pisum. Here, we test the hypothesis that ApNEAAT1 is localized to the symbiotic interface during asexual embryogenesis. Results During A. pisum asexual embryogenesis, ApNEAAT1 does not localize to the symbiotic interface. We observed ApNEAAT1 localization to the maternal follicular epithelium, the germline, and, in late-stage embryos, to anterior neural structures and insect immune cells (hemocytes). We predict that ApNEAAT1 provisions non-essential amino acids to developing oocytes and embryos, as well as to the brain and related neural structures. Additionally, ApNEAAT1 may perform roles related to host immunity. Conclusions Our work provides further evidence that the embryonic and adult bacteriomes of asexual A. pisum are not equivalent. Future research is needed to elucidate the developmental time point at which the bacteriome reaches maturity.

scholarly journals Extensive Proliferation of Transposable Elements in Heritable Bacterial Symbionts

2007 ◽  
Vol 190 (2) ◽  
pp. 777-779 ◽  
Author(s):  
Gordon R. Plague ◽  
Helen E. Dunbar ◽  
Phat L. Tran ◽  
Nancy A. Moran
Keyword(s):  
Transposable Elements ◽  
Insertion Sequence ◽  
Early Stage ◽  
Bacterial Symbionts ◽  
Is Elements ◽  
Bacterial Endosymbionts ◽  
Genomic Recombination

ABSTRACT We found that insertion sequence (IS) elements are unusually abundant in the relatively recently evolved bacterial endosymbionts of maize weevils. Because multicopy elements can facilitate genomic recombination and deletion, this IS expansion may represent an early stage in the genomic reduction that is common in most ancient endosymbionts.

Age, gut location and diet impact the gut microbiome of a tropical herbivorous surgeonfish

2019 ◽  
Author(s):  
Lara Parata ◽  
Shaun Nielsen ◽  
Xing Xing ◽  
Torsten Thomas ◽  
Suhelen Egan ◽  
...  
Keyword(s):  
Coral Reef ◽  
Gastrointestinal Tract ◽  
Bacterial Community ◽  
Gut Microbiota ◽  
Bacterial Communities ◽  
Food Source ◽  
Amplicon Sequencing ◽  
Rrna Gene ◽  
Bacterial Symbionts ◽  
Adult Fish

Abstract Herbivorous fishes play important ecological roles in coral reefs by consuming algae that can otherwise outcompete corals, but we know little about the gut microbiota that facilitates this process. This study focussed on the gut microbiota of an ecologically important coral reef fish, the convict surgeonfish Acanthurus triostegus. We sought to understand how the microbiome of this species varies along its gastrointestinal tract and how it varies between juvenile and adult fish. Further, we examined if the bacteria associated with the diet consumed by juveniles contributes to the gut microbiota. 16S rRNA gene amplicon sequencing showed that bacterial communities associated with the midgut and hindgut regions were distinct between adults and juveniles, however, no significant differences were seen for gut wall samples. The microbiota associated with the epilithic algal food source was similar to that of the juvenile midgut and gut wall but differed from the microbiome of the hindgut. A core bacterial community including members of taxa Epulopiscium and Brevinemataceae was observed across all gastrointestinal and diet samples, suggesting that these bacterial symbionts can be acquired by juvenile convict surgeonfish horizontally via their diet and then are retained into adulthood.

scholarly journals Ploidy dynamics in aphid host cells harboring bacterial symbionts

2021 ◽  
Author(s):  
Tomonari Nozaki ◽  
Shuji Shigenobu
Keyword(s):  
Acyrthosiphon Pisum ◽  
Biological Significance ◽  
Large Cell ◽  
Host Cells ◽  
Bacterial Symbionts ◽  
Buchnera Aphidicola ◽  
Ploidy Levels ◽  
Future Studies ◽  
Functional Roles ◽  
Aphid Host

AbstractAphids have evolved bacteriocytes or symbiotic host cells that harbor the obligate mutualistic bacterium Buchnera aphidicola. Because of the large cell size (approximately 100 μm in diameter) of bacteriocytes and their pivotal role in nutritional symbiosis, researchers have considered that these cells are highly polyploid and assumed that bacteriocyte polyploidy may be essential for the symbiotic relationship between the aphid and the bacterium. However, little is known about the ploidy levels and dynamics of aphid bacteriocytes. Here, we quantitatively analyzed the ploidy levels in the bacteriocytes of the pea-aphid Acyrthosiphon pisum. Image-based fluorometry revealed the hyper polyploidy of the bacteriocytes ranging from 16- to 256-ploidy throughout the lifecycle. Bacteriocytes of adult parthenogenetic viviparous females were mainly 64-128C DNA levels, while those of sexual morphs (oviparous females and males) were consisted of 64C, and 32-64C cells, respectively. During post-embryonic development of viviparous females, the ploidy level of bacteriocytes increased substantially, from 16-32C at birth to 128-256C in actively reproducing adults. These results suggest that the ploidy levels are dynamically regulated among phenotypes and during development. Our comprehensive and quantitative data provides a foundation for future studies to understand the functional roles and biological significance of the polyploidy of insect bacteriocytes.

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