Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses: a systematic review and meta-analysis

FEMS Microbiology Letters, Год журнала: 2019, Номер 366(3)

Опубликована: Янв. 15, 2019

Symbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. The rates distributions modes have not been thoroughly investigated across associations, despite their consequences on symbiont host evolution. To address this empirically, I compiled data from the literature bacteria-multicellular eukaryote for which mode was available. Of total 528 analyzed symbioses, 21.2% were strictly horizontally transmitted, 36.0% exhibited some form mixed 42.8% vertically transmitted. Controlling phylogenetically independent symbiosis events revealed approximately equally distributed among 113 at 32.1%+/-0.57% horizontal, 37.8%+/-1.4% 31.1%+/-1.3% vertical transmission. Binning symbioses by environment an abundance land lack it in aquatic environments. naturally occurring uneven distribution taxa environments prevented controlling host/symbiont phylogeny. However, results robust over large number independently evolved suggesting that many transmitted are capable barriers exist reduce rate horizontal events. Thus, both type influence

Язык: Английский

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Beetle–Bacterial Symbioses: Endless Forms Most Functional

Annual Review of Entomology, Год журнала: 2021, Номер 67(1), С. 201 - 219

Опубликована: Окт. 4, 2021

Beetles are hosts to a remarkable diversity of bacterial symbionts. In this article, we review the role these partnerships in promoting beetle fitness following surge recent studies characterizing symbiont localization and function across Coleoptera. Symbiont contributions range from supplementation essential nutrients digestive or detoxifying enzymes production bioactive compounds providing defense against natural enemies. Insights on functional highlight how symbiosis can expand host's ecological niche, but also constrain its evolutionary potential by specialization. As differ within between clades, discuss it corresponds microbe's beneficial outline molecular behavioral mechanisms underlying translocation transmission holometabolous host. reviewing literature, emphasize study inform our understanding phenotypic innovations behind success beetles.

Язык: Английский

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Parallel Evolution in the Integration of a Co-obligate Aphid Symbiosis

Current Biology, Год журнала: 2020, Номер 30(10), С. 1949 - 1957.e6

Опубликована: Апрель 2, 2020

•Aphids have independently evolved dependence on Serratia symbiotica at least 4 times•The integration of the new co-obligate symbiont proceeds in a predictable manner•Loss riboflavin and peptidoglycan pathways Buchnera leads to co-dependence•Amino acid synthesis is taken over by second phase complementarity Insects evolve dependence—often extreme—on microbes for nutrition. This includes cases which insects harbor multiple endosymbionts that function collectively as metabolic unit [1McCutcheon J.P. McDonald B.R. Moran N.A. Convergent evolution roles bacterial co-symbionts insects.Proc. Natl. Acad. Sci. USA. 2009; 106: 15394-15399Crossref PubMed Scopus (232) Google Scholar, 2McCutcheon von Dohlen C.D. An interdependent patchwork nested symbiosis mealybugs.Curr. Biol. 2011; 21: 1366-1372Abstract Full Text PDF (217) 3Takiya D.M. Tran P.L. Dietrich C.H. Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) their dual symbionts.Mol. Ecol. 2006; 15: 4175-4191Crossref (130) 4Wu D. Daugherty S.C. Van Aken S.E. Pai G.H. Watkins K.L. Khouri H. Tallon L.J. Zaborsky J.M. Dunbar H.E. et al.Metabolic genomics sharpshooters.PLoS 4: e188Crossref (309) 5Rao Q. Rollat-Farnier P.A. Zhu D.T. Santos-Garcia Silva F.J. Moya A. Latorre Klein C.C. Vavre F. Sagot M.F. al.Genome reduction potential complementation whitefly Bemisia tabaci.BMC Genomics. 2015; 16: 226Crossref (57) Scholar]. How do these dependences originate [6Douglas A.E. multi-partner endosymbioses function.Nat. Rev. Microbiol. 2016; 14: 731-743Crossref (66) Scholar], there sequence events leading symbionts? While symbioses, hosts rely nutrient-provisioning symbionts, numerous times across sap-feeding insects, only one known case aphids, involving aphidicola Lachninae subfamily [7Pérez-Brocal V. Gil R. Ramos S. Lamelas Postigo M. Michelena A small microbial genome: end long symbiotic relationship?.Science. 314: 312-313Crossref (257) 8Lamelas Pérez-Brocal Gómez-Valero L. Gosalbes M.J. Evolution secondary "Candidatus serratia symbiotica" aphid species lachninae.Appl. Environ. 2008; 74: 4236-4240Crossref (60) 9Manzano-Marín Simon J.C. Reinventing wheel making it round again: evolutionary convergence Buchnera-serratia consortia between distantly related aphids Tuberolachnus salignus Cinara cedri.Genome Evol. 8: 1440-1458Crossref (40) Here, we identify additional independent transitions same different aphids. Comparing recent ancient associations allow us investigate intermediate stages anatomical Serratia. We find uniquely replicated support idea initiate manner—through parallel processes. Specifically, show how repeated losses lead then provide evidence stepwise process integration, whereby evolves first. Then, essential amino are lost (at ∼30–60 mya), coincides with increased companion symbiont. Finally, demonstrate can ahead specialized structures (e.g., bacteriocytes), no direct nutritional basis. More generally, our results suggest energetic costs synthesizing nutrients may unified explanation gene occur during symbiosis. Sap-feeding provided elegant studies organisms unit. These include mealybugs depend endosymbionts, turn own cicadas, has fragmented into distinct but lineages What processes drive join symbioses and, more predictable, deterministic genomic The an ideal lineage study early-stage symbioses. majority single obligate symbiont, aphidicola, non-obligate (hereafter referred Serratia, respectively). found frequencies species, transitioned relationship Such functioning marked Buchnera's losing capabilities, namely ability synthesize some tryptophan [10Manzano-Marín Settling down: genome from tujafilina zooms accommodation cooperative intracellular life.Genome 2014; 6: 1683-1698Crossref (47) Our aim was determine whether (1) other co-dependences arisxen (2) ask followed genomic, metabolic, trajectories. patterns insight led structure Using data prevalence 131 [11Henry L.M. Maiden M.C.J. Ferrari J. Godfray H.C.J. Insect life history mutualism.Ecol. Lett. 18: 516-525Crossref (90) identified carry high frequency, tested populations both United Kingdom Netherlands defined having reliance if all individuals within they experience significant fitness when removed. Symbionts not meet criteria "facultative," host survival. screened presence using PCR measured "curing" individual antibiotics selectively removed without affecting Buchnera, counted total offspring lifetime fecundity absence ubiquitous seven (Table S1), representing Microlophium carnosum, Aphis urticata, Periphyllus genus. In genus, consistently present five surveyed, confirmed via curing P. hirticornis lyropictus. transition origins genus (see below). Curing had most dramatic effect potentially reflecting longer-term association (Figure 1A). antibiotic treatments control Acyrthosiphon pisum, harbors facultative uninfected Macrosiphoniella artemisiae (Figures 1A S1; Data S1A). Likewise, qPCR treatment reduced density 1B; S1B), did reduce 1C; S1B). next estimated deep coverage 16S amplicon sequencing field-collected previous First, genus: absent Chaitophorus sister clade (Data S1C). suggests originated divergence 2 genera 63–79 mya S2). Second, (<30 mya) urticata carnosum. either or infection idaei fabae urticata. Lack likewise Macrosiphum euphorbiae asked evolving associated consistent signature specifically Buchnera-Serratia originates manner lineages. obtained whole-genome urticatasymbiont; aphid; co-obligate;Serratia symbiotica;Buchnera aphidicola; dependence; complementation, species. used previously published (Cinara cedri, C. salignus) compare four included here, subfamily. analysis centered genes involved nutrient provisioning S1D). focused experimental being aphid: [14Nakabachi Ishikawa Provision aphid, endosymbiotic bacteria, Buchnera.J. Physiol. 1999; 45: 1-6Crossref (91) Scholar] acids [15Douglas Prosser W.A. Synthesis pea (Acyrthosiphon pisum) symbiosis.J. 1992; 38: 565-568Crossref (172) 16Douglas Sulphate utilization symbiosis.Insect Biochem. 1988; 599-605Crossref (61) 17Febvay G. Liadouze I. Guillaud Bonnot Analysis metabolism pisum: multidimensional approach aphids.Arch. 1995; 29: 45-69Crossref (78) 18Liadouze Febvay Metabolic fate aposymbiotic pisum (Harris) (Homoptera: Aphididae).Symbiosis. 1996; 115-127Google 19Brinza Viñuelas Cottret Calevro Rahbé Y. Duport Colella Rabatel Gautier al.Systemic primary endosymbiont pisum.C. 332: 1034-1049Crossref (33) 20Wilson A.C.C. Ashton P.D. Charles Jander Kushlan P.F. Macdonald S.J. Schwartz J.F. al.Genomic relations its bacterium aphidicola.Insect Mol. 2010; 19: 249-258Crossref (147) 21Shigenobu Wilson Genomic revelations mutualism: symbiont.Cell. Life 68: 1297-1309Crossref (92) Of particular interest pathway loss this been hypothesized trigger carnosum 3). missing gene, part ribD complex, pathway. contrast, full missing, Previous work also capacity certain cedri T. salignus). similar lineage. pseudogenized, orthologous copies, predicted serve function, retained Conversely, genomes relationships. result advanced stage functional further supported several appear complete surprising, given consistency co-obligately dependent Compared sole (A. Myzus persicae, glycines), six copies None links Table S2 detail). arise system through alternative starting points, including non-nutritional pathways. General features strains hypothesis compared S3). Both size GC content highly clades, suggestive degree degradation. Gene redundancies indicative age associations. still contain number (72.5% 39.2%, lineages, acericola aceris 11.5% redundancy two symbionts. lyropictus, 47.1% overlap. higher lyropictus likely due recently replaced another strain As could nutrition, investigated translation, underlies functions bacteria [22Gil Peretó Determination core minimal set.Microbiol. 2004; 518-537Crossref (402) synthesis, shown be important systems [23Bublitz D.C. Chadwick G.L. Magyar J.S. Sandoz K.M. Brooks Mesnage Ladinsky M.S. Garber A.I. Bjorkman P.J. Orphan V.J. McCutcheon Peptidoglycan Production Insect-Bacterial Mosaic.Cell. 2019; 179: 703-712.e7Abstract (29) precursors chorismate, homoserine, vitamins B5 B9, lipoic acid. B showed riboflavin. However, (B5 Lachninae) where symbionts (B9 pisum), so unclear Genes were conserved S1E). peptidoglycan, however, entirely (Lachninae aphids). cases, genomes. because contributing role addition providing host. murF. pseudogenized glycines, any than Buchnera. Lastly, studied abundance localization look signatures expected greater would correspond integration—for example, formation organ (bacteriome) house To test idea, performed fluorescent situ hybridization (FISH) probes targeting predicted, corresponding 4). extreme case, large containing bacteriocytes abdomens contrast exhibit localized cluster relatively cells (∼4), forming bacteriome surrounded Buchnera-containing bacteriocytes. integrated, sheath surrounding pattern maintains increase takes metabolically demanding role. quantify aphid. line predictions, substantial coincided acids. ratio dramatically 512:1 hirticornis. 3:1 less integrated 1B). Dependence eukaryotes. vast ancient. needed reveal steps observed By comparing strong mechanisms initially binding partners relationships deterministic, manner. trajectories FISH occurring 30 60 million years after evolves. characterized partnerships adopted first repeatedly produce each lost, compensate changes Studies aphid's demand low nutrients, such 24Sasaki Hayashi Growth reproduction maintained artificial diets.J. 1991; 37: 749-756Crossref 25Russell C.W. Poliakov Haribal van Wijk K.J. Douglas Matching supply animal host.Proc. 281: 20141163Crossref explain why modest vitamin easily met even abundance. sub-family, missing. once established, follow

Язык: Английский

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Microbiome breeding: conceptual and practical issues

Trends in Microbiology, Год журнала: 2022, Номер 30(10), С. 997 - 1011

Опубликована: Май 18, 2022

Язык: Английский

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Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

The ISME Journal, Год журнала: 2023, Номер 17(11), С. 1798 - 1807

Опубликована: Сен. 2, 2023

Abstract Microbes can be an important source of phenotypic plasticity in insects. Insect physiology, behaviour, and ecology are influenced by individual variation the microbial communities held within insect gut, reproductive organs, bacteriome, other tissues. It is becoming increasingly clear how microbiome for fitness, expansion into novel ecological niches, environments. These investigations have garnered heightened interest recently, yet a comprehensive understanding intraspecific assembly function these insect-associated shape insects still lacking. Most research focuses on core associated with species ignores variation. We argue that among driver evolution, we provide examples showing such influence fitness health insects, invasions, their persistence new environments, responses to global environmental changes.

Язык: Английский

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