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The Genomics and Evolution of Mutualistic and Pathogenic Bacteria

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The Genomics and Evolution of Mutualistic and Pathogenic Bacteria Symbiotic bacteria in animals • Oct 3 2006 • Nancy Moran • Professor, Ecology and Evolutionary Biology Reading: The gut flora as a forgotten organ by A. O’Hara and F Shanahan EMBO Reports. 2006 What is symbiosis? • Term typically used for a chronic association of members of more than one genetic lineage, without overt pathogenesis • Often for mutual benefit, which may be easy or difficult to observe – Exchange of nutrients or other metabolic products, protection, transport, structural integrity Microbes in animal evolution • Bacteria present by 3.9 bya, Archaea and Eukaryota by >2 bya – The Earth is populated by ecologically diverse microbes • Animals appear about 1 bya • Animals evolved in microbial soup – “Innate” immune system probably universal among animal phyla: pathogenic infection was a constant selection pressure – But animals also evolved codependence on microbes, some of which are required for normal development and reproduction evolutionary innovations through symbiosis: examples • Eukaryotic cell (mitochondria) • Photosynthesis in eukaryotes (plastids) • Colonization of land by plants (mycorrhizae) • Nitrogen fixation by plants (rhizobia) • Animal life at deep sea vents (chemoautotrophic life systems) • Use of many nutrient-limited niches by animal lineages Why do hosts and symbionts cooperate so often? • Persistent association allows both to increase their persistence and replication. –Coinheritance – Long-term infection • Intimate metabolic exchange generating immediate beneficial feedback Symbiosis- main variables • Route of infection (maternal, horizontal, mixture) • Mechanisms of benefiting or exploiting hosts • Location of symbionts in host body: – intracellular, between cells, in specialized organ or in other tissues, within gut lumen, etc. • Molecular mechanisms of invading host tissues or cells: similarities and differences between symbionts and pathogens Routes of transmission • Vertical (parent to offspring) • Horizontal – May live in the environment (outside hosts), or not • Mixture of vertical and horizontal – Eg acquire from other individuals in the same family or colony (termites, humans… ) Termite with gut removed Diverse microbes in termite gut •Vertical transmission (parent to offspring) –Infection of eggs, seeds, embryos, or babies –Usually maternal only –Has evolved in many invertebrate symbioses with bacteria, viruses and fungi –Can be transovariolar (within the mother’s body) or some other route (e.g. fecal-oral for gut inhabitants) Ways that vertically transmitted microbes can increase in frequency • Increase host survival & reproduction (mutualism) • “Reproductive manipulation” – Turn presumptive male hosts into females –Cause all-female progeny so that all offspring are carriers (“son-killers”) – Cause hosts to be parthenogenetic (all female) – Cytoplasmic incompatibility: infected males sterilize uninfected females – All of these are known to occur--caused by bacterial symbionts in insects: “Wolbachia” and spiroplasmas Ways that vertically transmitted microbes can increase in frequency • Increase host survival & reproduction (mutualism) – Very common Why might vertical transmission be associated with mutualistic effects on hosts? • Most famous cases are the lineages leading to organelles – Mitochondria evolved from the alpha-Proteobacteria about 2 billion years ago – Chloroplasts evolved from cyanobacteria about 1 billion years ago Vertically transmitted symbiont can ultimately fuse with the host to form a “super-organism” --mutually obligate relationship --very unlike pathogens Eukaryotic genomes are littered with hundreds of genes from mitochondria and plastids--now apparent from plant and animal genome sequences. (Phylogenetic evidence for gene transfer from organelles) Cyanobacteria Cyanobacteria Eukaryote- Plant Cyanobacteria Bacteria Bacteria Bacteria Bacteria Eukaryote-protozoan Eukaryote-protozoan Eukaryote-animal Eukaryote-fungal e.g. Arabidopsis genome has >1000 genes from cyanobacteria Vertically transmitted bacteria in animal hosts--2 examples 1 Insect-nutritional mutualists (aphids and Buchnera) 2 Symbionts providing defense against natural enemies of hosts Beneficial microbes in animal hosts--examples 1 Insect-nutritional mutualists (aphids & Buchnera) Many invertebrates have specialized intracellular associations with bacteria that make nutrients Examples: marine bivalves, leeches, many insects Metazoa: ancestral loss of many genes underlying biosynthesis of compounds essential for metabolism, including many amino acids and many cofactors. -->dietary requirements. Little or no gene uptake Tree of Life, N. Pace Aphids-Buchnera • Intracellular bacteria in specialized host cells • Vertically transmitted-mother to offspring • Infection dates to >100 million years • Rather closely related to E. coli, but genome much reduced (only 600 of ~4000 ancestral genes retained) • Provides nutrients to host, allowing use of a diet that otherwise would be inadequate. maternal bacteriocytes late embryos containing symbionts early embryos with symbionts visible 1 mm J. Sandström Buchnera aphidicola within pea aphid bacteriocyte 1µm J. White Aphid eggs containing Buchnera from mother Buchnera from mother 0.5 mm A. Mira host aphid gene phylogeny Buchnera gene phylogeny Aphididae Uroleucon & relatives Pemphigus betae Acyrthosiphon pisum origin of Schlectendalia chinensis Macrosiphum rosae symbiosis Uroleucon erigeronense Melaphis rhois Uroleucon caligatum Chaitophorus viminalis Uroleucon rurale Uroleucon helianthicola Mindarus kinseyi Uroleucon jaceicola Uroleucon sonchi Uroleucon obscurum Acyrthosiphon pisum Uroleucon rapunculoides Uroleucon sonchi Macrosiphum rosae colonization Uroleucon solidaginis Myzus persicae of Asteraceae Uroleucon jaceae <20 Mya Uroleucon aeneum Rhopalosiphum padi ancestor of Uroleucon rudbeckiae extant aphids Schizaphis graminum 100-200 Mya Uroleucon astronomus Rhopalosiphum maidis Uroleucon ambrosiae ->Strict vertical transmission since ancient infection of ancestral host Aphid stylet sheaths in phloem sieve tubes Schizaphis graminum on barley 70.0% 60.0% % of total amino acids in phloem 50.0% sap of 6 angiosperms broad beans 40.0% bird cherry sonchus alfalfa barley 30.0% barley2 Essential nutrients for animals wheat 20.0% 10.0% 0.0% ILE HIS ALA LYS VAL LEU ASP TYR TRP GLY ASN SER CYS PHE THR GLN GLU MET PRO ARG trp plasmid in Buchnera (Schizaphis graminum) = genomic adaptation to make more nutrients for hosts ori trpE chorismate trpG trpG trpE trpEG ori anthranilate synthase plasmid 14.3 kb ori trpE trpG trpG trpE ori anthranilate tryptophan chromosome trpD trpC(F) trpB trpA Lai, Baumann & Baumann PNAS 1994 The Buchnera gene set (570 genes) is a subset of that of E. coli (~4500 genes) Shigenobu et al 2000 Nature Essential amino acid biosynthetic pathways Nonessential amino acid biosynthetic pathways argA argB argC argD argE carAB argF argG argH tyrA tyrA hisC Glutamate---> ---> ---> ---> ---> Ornithine ---> ---> ---> ---> ARG Chorisimate ---> ---> ---> TYR ilvHI ilvC ilvD ilvE proB proA proC Pyruvate ---> ---> ---> ---> VAL Glutamate ---> ---> ---> PRO ilvA ilvHI ilvC ilvD ilvE serA serC serB Threonine ---> a-Ketobutyrate ---> ---> ---> ---> ILE 3-Phosphoglycerate ---> ---> ---> SER + Pyruvate glyA ilvHI ilvC ilvD leuA leuCD leuB ilvE Serine ---> GLY Pyruvate ---> ---> ---> ---> ---> ---> ---> LEU cysE cysK aroH aroB aroD aroE aroK aroA aroC Serine ---> ---> CYS PEP+Erythrose ---> ---> ---> ---> ---> ---> ---> Chorismate 4-Phosphate gtBD/gdhA 2-oxoglutarate ---> GLU pheA pheA hisC Chorismate ---> ---> ---> PHE glnA Glutamate ---> GLN trpEG trpD trpC trpC trpAB Chorismate ---> ---> ---> ---> ---> TRP aspC+tyrB Oxaloacetate ---> ASP thrA asd thrA thrB thrC asnB/asnA Aspartate ---> ---> ---> Homoserine ---> ---> THR Aspartate ---> ASN metB metC metE Homoserine ---> ---> ---> MET alaB/avtA Pyruvate ---> ALA thrA asd dapA dapB dapD dapC dapE dapF lysA Aspartate ---> ---> ---> ---> ---> ---> ---> ---> ---> LYS hisG hisI hisA hisHF hisB hisC hisB hisD PRPP + ATP ---> ---> ---> ---> ---> ---> ---> ---> HIS GENE / product present in Buchnera GENE / product absent in Buchnera (based on Shigenobu et al 2000) But other symbionts appear not to Eukaryotic genomes contain have not left a legacy of many many genes from organelles, genes transferred to host apparent from eukaryotic genomes, at least not in animals so genome sequences. far sequenced (e.g., Drosophila) Why this difference? Heritable mutualistic bacteria (maternal transmission) Not much like pathogens-host has •Mitochondria taken over mechanisms of invading • Chloroplasts host cells and has coevolved to • Obligate “nutritional” symbionts (e.g. maintain the association Buchnera in aphids) • Facultative maternally transmitted Much more like pathogens--have symbionts to invade naïve hosts, overcome immune responses, but typically benefit hosts Similarities between facultative symbionts and pathogens at the molecular level • Use of toxins that target eukaryotic cells and manipulate the cell cycle • Use of secretion systems that deliver effector molecules to the host cytoplasm, sometimes enable host cell invasion – Eg Type III Secretion Systems used by Salmonella and Yersinia pestis (mammalian pathogens) and by mutualistic symbionts of animals and plants • Similar trends in genome evolution: proliferation of insertion sequences (transposable elements) and inactivation of many ancestral genes Mutualistic effects of facultative symbionts on aphids Experiments comparing pea aphids with the same genotype but differing
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