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 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 Two Deoxythymidine Triphosphate Synthesis-Related Genes Regulate Obligate Symbiont Density and Reproduction in the Whitefly Bemisia tabaci MED

2021 ◽  
Vol 11 ◽  
Author(s):  
Zezhong Yang ◽  
Cheng Gong ◽  
Yuan Hu ◽  
Jie Zhong ◽  
Jixing Xia ◽  
...  
Keyword(s):  
Amino Acid ◽  
Rna Interference ◽  
Bemisia Tabaci ◽  
Essential Amino Acid ◽  
Cellular Growth ◽  
Capacity Analysis ◽  
Host Insect ◽  
Obligate Symbiont ◽  
Pyrimidine Pathway

Deoxythymidine triphosphate (dTTP) is essential for DNA synthesis and cellular growth in all organisms. Here, genetic capacity analysis of the pyrimidine pathway in insects and their symbionts revealed that dTTP is a kind of metabolic input in several host insect/obligate symbiont symbiosis systems, including Bemisia tabaci MED/Candidatus Portiera aleyrodidarum (hereafter Portiera). As such, the roles of dTTP on both sides of the symbiosis system were investigated in B. tabaci MED/Portiera. Dietary RNA interference (RNAi) showed that suppressing dTTP production significantly reduced the density of Portiera, significantly repressed the expression levels of horizontally transferred essential amino acid (EAA) synthesis-related genes, and significantly decreased the reproduction of B. tabaci MED adults as well as the hatchability of their offspring. Our results revealed the regulatory role of dTTP in B. tabaci MED/Portiera and showed that dTTP synthesis-related genes could be potential targets for controlling B. tabaci as well as other sucking pests.

scholarly journals Methylation at CpG sites in genomes of aphid Acyrtosiphon pisum and its endosymbiont Buchnera

2021 ◽  
Author(s):  
Mathilde Clement ◽  
Martine Da Rocha ◽  
Sandra Agnel ◽  
Guenter Raddatz ◽  
Alain Robichon ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Buchnera Aphidicola ◽  
Low Level ◽  
Endosymbiotic Bacteria ◽  
Whole Genomes ◽  
Dna Methylase ◽  
Mutualistic Relationship ◽  
Sap Feeding ◽  
Methyl Cytosine ◽  
Methylation Patterns

Pea aphid Acyrtosiphon pisum, a sap-feeding insect, has established a mutualistic relationship with an endosymbiotic bacteria (Buchnera aphidicola) that constitutes an evolutionary successful symbiosis to synthetize complex chemical compounds from a nutrient deprived diet. In this study, led by the presence of DNMT1 and a putative DNMT3 methylase in the aphid genome, we investigated the distribution of the methyl groups on 5'cytosine in CpG motifs on the whole genomes of host and endosymbiont, and looked into their correlation with gene expression. The DNA methylation turned to be present at low level in aphid (around 3% of total genomic cytosine) compared to mammals and plants, but increased to ~9% in genes. Interestingly, the reduced genome of the endosymbiont Buchnera also shows global low level of methyl cytosine despite the fact that its genome does not shelter any DNA methylase. This finding argues for the import of DNA methylase from the host to the endosymbiont. The observed differences in methylation patterns between two clonal variants (host plus endosymbiont) are reported along with the differences in their transcriptome profiles. Our data allowed to decipher a dynamic combinatorial DNA methylation and epigenetic cross talk between host and symbiont in a clonality context that might count for the aphid adaptation to environment.

scholarly journals New Insights on the Evolutionary History of Aphids and Their Primary Endosymbiont Buchnera aphidicola

2011 ◽  
Vol 2011 ◽  
pp. 1-9 ◽  
Author(s):  
Vicente Pérez-Brocal ◽  
Rosario Gil ◽  
Andrés Moya ◽  
Amparo Latorre
Keyword(s):  
Generation Time ◽  
Evolutionary History ◽  
Parallel Evolution ◽  
Aphid Species ◽  
Evolutionary Analysis ◽  
Buchnera Aphidicola ◽  
Genomic Features ◽  
Evolutionary Pattern ◽  
History Of ◽  
Molecular Evolutionary Analysis

Since the establishment of the symbiosis between the ancestor of modern aphids and their primary endosymbiont, Buchnera aphidicola, insects and bacteria have coevolved. Due to this parallel evolution, the analysis of bacterial genomic features constitutes a useful tool to understand their evolutionary history. Here we report, based on data from B. aphidicola, the molecular evolutionary analysis, the phylogenetic relationships among lineages and a comparison of sequence evolutionary rates of symbionts of four aphid species from three subfamilies. Our results support previous hypotheses of divergence of B. aphidicola and their host lineages during the early Cretaceous and indicate a closer relationship between subfamilies Eriosomatinae and Lachninae than with the Aphidinae. They also reveal a general evolutionary pattern among strains at the functional level. We also point out the effect of lifecycle and generation time as a possible explanation for the accelerated rate in B. aphidicola from the Lachninae.

scholarly journals Regulation of Transcription in a Reduced Bacterial Genome: Nutrient-Provisioning Genes of the Obligate Symbiont Buchnera aphidicola

2005 ◽  
Vol 187 (12) ◽  
pp. 4229-4237 ◽  
Author(s):  
Nancy A. Moran ◽  
Helen E. Dunbar ◽  
Jennifer L. Wilcox
Keyword(s):  
Amino Acid ◽  
Acid Content ◽  
Acyrthosiphon Pisum ◽  
Bacterial Genome ◽  
Amino Acid Content ◽  
Transcript Abundance ◽  
Regulation Of Transcription ◽  
Buchnera Aphidicola ◽  
Obligate Symbiont ◽  
Dietary Amino Acid

ABSTRACT Buchnera aphidicola, the obligate symbiont of aphids, has an extremely reduced genome, of which about 10% is devoted to the biosynthesis of essential amino acids needed by its hosts. Most regulatory genes for these pathways are absent, raising the question of whether and how transcription of these genes responds to the major shifts in dietary amino acid content encountered by aphids. Using full-genome microarrays for B. aphidicola of the host Schizaphis graminum, we examined transcriptome responses to changes in dietary amino acid content and then verified behavior of individual transcripts using quantitative reverse transcriptase PCR. The only gene showing a consistent and substantial (>twofold) response was metE, which underlies methionine biosynthesis and which is the only amino acid biosynthetic gene retaining its ancestral regulator (metR). In another aphid host, Acyrthosiphon pisum, B. aphidicola has no functional metR and shows no response in metE transcript levels to changes in amino acid concentrations. Thus, the only substantial transcriptional response involves the one gene for which an ancestral regulator is retained. This result parallels that from a previous study on heat stress, in which only the few genes retaining the global heat shock promoter showed responses in transcript abundance. The irreversible losses of transcriptional regulators constrain ability to alter gene expression in the context of environmental fluctuations affecting the symbiotic partners.

Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola

2013 ◽  
Vol 68 (1) ◽  
pp. 42-54 ◽  
Author(s):  
Eva Nováková ◽  
Václav Hypša ◽  
Joanne Klein ◽  
Robert G. Foottit ◽  
Carol D. von Dohlen ◽  
...  
Keyword(s):  
Buchnera Aphidicola ◽  
Obligate Symbiont

scholarly journals Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae

2009 ◽  
Vol 75 (16) ◽  
pp. 5328-5335 ◽  
Author(s):  
Gaelen R. Burke ◽  
Benjamin B. Normark ◽  
Colin Favret ◽  
Nancy A. Moran
Keyword(s):  
Phylogenetic Analysis ◽  
Environmental Stresses ◽  
Endosymbiotic Bacteria ◽  
Obligate Symbiont ◽  
High Incidence ◽  
Serratia Symbiotica ◽  
And Function

ABSTRACT Many aphids harbor a variety of endosymbiotic bacteria. The functions of these symbionts can range from an obligate nutritional role to a facultative role in protecting their hosts against environmental stresses. One such symbiont is “Candidatus Serratia symbiotica,” which is involved in defense against heat and potentially also in aphid nutrition. Lachnid aphids have been the focus of several recent studies investigating the transition of this symbiont from a facultative symbiont to an obligate symbiont. In a phylogenetic analysis of Serratia symbionts from 51 lachnid hosts, we found that diversity in symbiont morphology, distribution, and function is due to multiple independent origins of symbiosis from ancestors belonging to Serratia and possibly also to evolution within distinct symbiont clades. Our results do not support cocladogenesis of “Ca. Serratia symbiotica” with Cinara subgenus Cinara species and weigh against an obligate nutritional role. Finally, we show that species belonging to the subfamily Lachninae have a high incidence of facultative symbiont infection.

scholarly journals Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

2015 ◽  
Vol 112 (33) ◽  
pp. 10169-10176 ◽  
Author(s):  
Gordon M. Bennett ◽  
Nancy A. Moran
Keyword(s):  
Extinction Risk ◽  
Rapid Evolution ◽  
Aphid Species ◽  
Buchnera Aphidicola ◽  
Short Run ◽  
Speciation Rates ◽  
Sap Feeding ◽  
Almost All ◽  
Host Genes ◽  
Ecological Range

Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host–symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host–pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphid–Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.

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 Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts

2016 ◽  
Author(s):  
A.S. Meseguer ◽  
A. Manzano-Marín ◽  
A. Coeur d’Acier ◽  
A-L. Clamens ◽  
M. Godefroid ◽  
...  
Keyword(s):  
Phylogenetic Analyses ◽  
Aphid Species ◽  
Buchnera Aphidicola ◽  
Evolutionary Transitions ◽  
Symbiotic Associations ◽  
Metabolic Functions ◽  
History Of ◽  
Serratia Symbiotica ◽  
Bacterial Genes

AbstractSymbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement and/or supplementation of an obligate symbiosis by an additional bacterium has occurred during the history of many insect groups. Yet, the factors favoring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a “ménage à trois”, in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species+confirm that these coresident symbionts fulfill essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that co-symbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

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