scholarly journals New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

2019 ◽  
Vol 85 (10) ◽  
Author(s):  
Inès Pons ◽  
François Renoz ◽  
Christine Noël ◽  
Thierry Hance

ABSTRACT Symbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study the mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains with a free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamics of cultivable S. symbiotica during the host’s lifetime using quantitative PCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Our study revealed that cultivable S. symbiotica bacteria are predisposed to establish a symbiotic association with a new aphid host, settling in its gut. We show that cultivable S. symbiotica bacteria colonize the entire aphid digestive tract following infection, after which the bacteria multiply exponentially during aphid development. Our results further reveal that gut colonization by the bacteria induces a fitness cost to their hosts. Nevertheless, it appeared that the bacteria also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica strains seem to be extracellularly transmitted, possibly through the honeydew, while S. symbiotica is generally considered a maternally transmitted bacterium living within the aphid body cavity and bringing some benefits to its hosts, despite its costs. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions. IMPORTANCE S. symbiotica is one of the most common symbionts among aphid populations and includes a wide variety of strains whose degree of interdependence on the host may vary considerably. S. symbiotica strains with a free-living capacity have recently been isolated from aphids. By using these strains, we established artificial associations by simulating new bacterial acquisitions involved in aphid gut infections to decipher their infection processes and biological effects on their new hosts. Our results showed the early stages involved in this route of infection. So far, S. symbiotica has been considered a maternally transmitted aphid endosymbiont. Nevertheless, we show that our cultivable S. symbiotica strains occupy and replicate in the aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, cultivable S. symbiotica bacteria are both parasites and mutualists given the context, as are many aphid endosymbionts. Our findings give new perception of the associations involved in bacterial mutualism in aphids.

2018 ◽  
Author(s):  
Pons Inès ◽  
Renoz François ◽  
Noël Christine ◽  
Hance Thierry

AbstractSymbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains having the possibility of free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamic of cultivable S. symbiotica strains during the host’s lifetime using qPCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Usually, S. symbiotica are considered as maternally-transmitted bacteria living within aphid body cavity and bringing some benefits to their hosts despite their costs. Otherwise, our study revealed that cultivable S. symbiotica are predisposed to establish a symbiotic association with new aphid host, settling in its gut. We showed that cultivable S. symbiotica colonized the entire aphid digestive tract following infection, after which the bacterium multiplied exponentially during aphid development. Our results further revealed that gut colonization by the bacteria induce a fitness cost to their hosts. Nevertheless, it appeared that they also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica seem to be extracellularly transmitted, possibly through the honeydew. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions.ImportanceFor the first time, our study provides experimental data that highlight a new kind of symbiotic associations in aphids. By successfully isolating microbial symbiont from aphids and by cultivating it in vitro in our laboratory, we established artificial association by simulating new bacterial acquisitions involved in aphid gut infection. Our results showed the early stages involved in this route of infection. Until now, Serratia symbiotica is considered as a maternally-transmitted aphid endosymbiont. Nevertheless, here, we showed that our cultivable strains having an intermediate status between a strict free-living bacterium and a facultative endosymbiont, occupy and replicate in aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, they are both parasites and mutualists given the context, as many of the endosymbionts in aphids. Our findings give new perception of associations involved in aphids’ symbiosis.


2019 ◽  
Vol 86 (1) ◽  
Author(s):  
Jessica H. Mitchell ◽  
Juliana M. Leonard ◽  
Jennifer Delaney ◽  
Peter R. Girguis ◽  
Kathleen M. Scott

ABSTRACT Use of hydrogen gas (H2) as an electron donor is common among free-living chemolithotrophic microorganisms. Given the presence of this dissolved gas at deep-sea hydrothermal vents, it has been suggested that it may also be a major electron donor for the free-living and symbiotic chemolithoautotrophic bacteria that are the primary producers at these sites. Giant Riftia pachyptila siboglinid tubeworms and their symbiotic bacteria (“Candidatus Endoriftia persephone”) dominate many vents in the Eastern Pacific, and their use of sulfide as a major electron donor has been documented. Genes encoding hydrogenase are present in the “Ca. Endoriftia persephone” genome, and proteome data suggest that these genes are expressed. In this study, high-pressure respirometry of intact R. pachyptila and incubations of trophosome homogenate were used to determine whether this symbiotic association could also use H2 as a major electron donor. Measured rates of H2 uptake by intact R. pachyptila in high-pressure respirometers were similar to rates measured in the absence of tubeworms. Oxygen uptake rates in the presence of H2 were always markedly lower than those measured in the presence of sulfide, as was the incorporation of 13C-labeled dissolved inorganic carbon. Carbon fixation by trophosome homogenate was not stimulated by H2, nor was hydrogenase activity detectable in these samples. Though genes encoding [NiFe] group 1e and [NiFe] group 3b hydrogenases are present in the genome and transcribed, it does not appear that H2 is a major electron donor for this system, and it may instead play a role in intracellular redox homeostasis. IMPORTANCE Despite the presence of hydrogenase genes, transcripts, and proteins in the “Ca. Endoriftia persephone” genome, transcriptome, and proteome, it does not appear that R. pachyptila can use H2 as a major electron donor. For many uncultivable microorganisms, omic analyses are the basis for inferences about their activities in situ. However, as is apparent from the study reported here, there are dangers in extrapolating from omics data to function, and it is essential, whenever possible, to verify functions predicted from omics data with physiological and biochemical measurements.


2021 ◽  
Vol 7 (6) ◽  
Author(s):  
Brenda S. Pratte ◽  
Teresa Thiel

Species of the floating, freshwater fern Azolla form a well-characterized symbiotic association with the non-culturable cyanobacterium Nostoc azollae, which fixes nitrogen for the plant. However, several cyanobacterial strains have over the years been isolated and cultured from Azolla from all over the world. The genomes of 10 of these strains were sequenced and compared with each other, with other symbiotic cyanobacterial strains, and with similar strains that were not isolated from a symbiotic association. The 10 strains fell into three distinct groups: six strains were nearly identical to the non-symbiotic strain, Nostoc ( Anabaena ) variabilis ATCC 29413; three were similar to the symbiotic strain, Nostoc punctiforme , and one, Nostoc sp. 2RC, was most similar to non-symbiotic strains of Nostoc linckia. However, Nostoc sp. 2RC was unusual because it has three sets of nitrogenase genes; it has complete gene clusters for two distinct Mo-nitrogenases and an alternative V-nitrogenase. Genes for Mo-nitrogenase, sugar transport, chemotaxis and pili characterized all the symbiotic strains. Several of the strains infected the liverwort Blasia, including N. variabilis ATCC 29413, which did not originate from Azolla but rather from a sewage pond. However, only Nostoc sp. 2RC, which produced highly motile hormogonia, was capable of high-frequency infection of Blasia. Thus, some of these strains, which grow readily in the laboratory, may be useful in establishing novel symbiotic associations with other plants.


2020 ◽  
Vol 9 (10) ◽  
Author(s):  
François Renoz ◽  
Jérôme Ambroise ◽  
Bertrand Bearzatto ◽  
Patrice Baa-Puyoulet ◽  
Federica Calevro ◽  
...  

Serratia symbiotica, one of the most frequent symbiont species in aphids, includes strains that exhibit various lifestyles ranging from free-living to obligate intracellular mutualism. Here, we report the draft genome sequences of two strains, namely, 24.1 and Apa8A1, isolated from aphids of the genus Aphis, consisting of genome sizes of 3,089,091 bp and 3,232,107 bp, respectively. These genome sequences may provide new insights into how mutualistic interactions between bacteria and insects evolve and are shaped.


2011 ◽  
Vol 77 (13) ◽  
pp. 4446-4454 ◽  
Author(s):  
Araceli Lamelas ◽  
María José Gosalbes ◽  
Andrés Moya ◽  
Amparo Latorre

ABSTRACTThe symbiotic association between aphids (Homoptera) andBuchnera aphidicola(Gammaproteobacteria) started about 100 to 200 million years ago. As a consequence of this relationship, the bacterial genome has undergone a prominent size reduction. The downsize genome process starts when the bacterium enters the host and will probably end with its extinction and replacement by another healthier bacterium or with the establishment of metabolic complementation between two or more bacteria. Nowadays, several complete genomes ofBuchnera aphidicolafrom four different aphid species (Acyrthosiphon pisum,Schizaphis graminum,Baizongia pistacea, andCinara cedri) have been fully sequenced.C. cedribelongs to the subfamily Lachninae and harbors two coprimary bacteria that fulfill the metabolic needs of the whole consortium:B. aphidicolawith the smallest genome reported so far and “CandidatusSerratia symbiotica.” In addition,Cinara tujafilina, another member of the subfamily Lachninae, closely related toC. cedri, also harbors “Ca.Serratia symbiotica” but with a different phylogenetic status than the one fromC. cedri. In this study, we present the complete genome sequence ofB. aphidicolafromC. tujafilinaand the phylogenetic analysis and comparative genomics with the otherBuchneragenomes. Furthermore, the gene repertoire of the last common ancestor has been inferred, and the evolutionary history of the metabolic losses that occurred in the different lineages has been analyzed. Although stochastic gene loss plays a role in the genome reduction process, it is also clear that metabolism, as a functional constraint, is also a powerful evolutionary force in insect endosymbionts.


2012 ◽  
Vol 78 (8) ◽  
pp. 2841-2849 ◽  
Author(s):  
Evan F. Goulden ◽  
Michael R. Hall ◽  
David G. Bourne ◽  
Lily L. Pereg ◽  
Lone Høj

ABSTRACTThe type strain ofVibrio owensii(DY05) was isolated during an epizootic of aquaculture-reared larvae (phyllosomas) of the ornate spiny lobster (Panulirus ornatus).V. owensiiDY05 was formally demonstrated to be the etiological agent of a disease causing rapid and reproducible larval mortality with pathologies similar to those seen during disease epizootics. Vectored challenge via the aquaculture live feed organismArtemia(brine shrimp) caused consistent cumulative mortality rates of 84 to 89% after 72 h, in contrast to variable mortality rates seen after immersion challenge. Histopathological examination of vector-challenged phyllosomas revealed bacterial proliferation in the midgut gland (hepatopancreas) concomitant with epithelial cell necrosis. A fluorescent-protein-labeledV. owensiiDY05 transconjugant showed dispersal of single cells in the foregut and hepatopancreas 6 h postexposure, leading to colonization of the entire hepatopancreas within 18 h and eventually systemic infection.V. owensiiDY05 is a marine enteropathogen highly virulent toP. ornatusphyllosoma that uses vector-mediated transmission and release from host association to a planktonic existence to perpetuate transfer. This understanding of the infection process will improve targeted biocontrol strategies and enhance the prospects of commercially viable larviculture for this valuable spiny lobster species.


2018 ◽  
Vol 7 (14) ◽  
Author(s):  
William G. Miller ◽  
Emma Yee ◽  
James L. Bono

Many Arcobacter spp. are free living and are routinely recovered from marine environments.


mBio ◽  
2013 ◽  
Vol 4 (4) ◽  
Author(s):  
Alanna M. Spees ◽  
Tamding Wangdi ◽  
Christopher A. Lopez ◽  
Dawn D. Kingsbury ◽  
Mariana N. Xavier ◽  
...  

ABSTRACTTreatment with streptomycin enhances the growth of human commensalEscherichia coliisolates in the mouse intestine, suggesting that the resident microbial community (microbiota) can inhibit the growth of invading microbes, a phenomenon known as “colonization resistance.” However, the precise mechanisms by which streptomycin treatment lowers colonization resistance remain obscure. Here we show that streptomycin treatment rendered mice more susceptible to the development of chemically induced colitis, raising the possibility that the antibiotic might lower colonization resistance by changing mucosal immune responses rather than by preventing microbe-microbe interactions. Investigation of the underlying mechanism revealed a mild inflammatory infiltrate in the cecal mucosa of streptomycin-treated mice, which was accompanied by elevated expression ofNos2, the gene that encodes inducible nitric oxide synthase. In turn, this inflammatory response enhanced the luminal growth ofE. coliby nitrate respiration in aNos2-dependent fashion. These data identify low-level intestinal inflammation as one of the factors responsible for the loss of resistance toE. colicolonization after streptomycin treatment.IMPORTANCEOur intestine is host to a complex microbial community that confers benefits by educating the immune system and providing niche protection. Perturbation of intestinal communities by streptomycin treatment lowers “colonization resistance” through unknown mechanisms. Here we show that streptomycin increases the inflammatory tone of the intestinal mucosa, thereby making the bowel more susceptible to dextran sulfate sodium treatment and boosting theNos2-dependent growth of commensalEscherichia coliby nitrate respiration. These data point to the generation of alternative electron acceptors as a by-product of the inflammatory host response as an important factor responsible for lowering resistance to colonization by facultative anaerobic bacteria such asE. coli.


Parasitology ◽  
2016 ◽  
Vol 143 (14) ◽  
pp. 1824-1846 ◽  
Author(s):  
DANIEL P. BENESH

SUMMARYComplex life cycles are common in free-living and parasitic organisms alike. The adaptive decoupling hypothesis postulates that separate life cycle stages have a degree of developmental and genetic autonomy, allowing them to be independently optimized for dissimilar, competing tasks. That is, complex life cycles evolved to facilitate functional specialization. Here, I review the connections between the different stages in parasite life cycles. I first examine evolutionary connections between life stages, such as the genetic coupling of parasite performance in consecutive hosts, the interspecific correlations between traits expressed in different hosts, and the developmental and functional obstacles to stage loss. Then, I evaluate how environmental factors link life stages through carryover effects, where stressful larval conditions impact parasites even after transmission to a new host. There is evidence for both autonomy and integration across stages, so the relevant question becomes how integrated are parasite life cycles and through what mechanisms? By highlighting how genetics, development, selection and the environment can lead to interdependencies among successive life stages, I wish to promote a holistic approach to studying complex life cycle parasites and emphasize that what happens in one stage is potentially highly relevant for later stages.


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