Modeling trophic dependencies and exchanges among insects’ bacterial symbionts in a host-simulated environment

BackgroundIndividual organisms are linked to their communities and ecosystems via metabolic activities. Metabolic exchanges and co-dependencies have long been suggested to have a pivotal role in determining community structure. In phloem-feeding insects such metabolic interactions with bacteria enable complementation of their deprived nutrition. The phloem-feeding whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) harbors an obligatory symbiotic bacterium, as well as varying combinations of facultative symbionts. This well-defined bacterial community in B. tabaci serves here as a case study for a comprehensive and systematic survey of metabolic interactions within the bacterial community and their associations with documented occurrences of bacterial combinations. We first reconstructed the metabolic networks of five common B. tabaci symbionts genera (Portiera, Rickettsia, Hamiltonella, Cardinium and Wolbachia), and then used network analysis approaches to predict: (1) species-specific metabolic capacities in a simulated bacteriocyte-like environment; (2) metabolic capacities of the corresponding species’ combinations, and (3) dependencies of each species on different media components.ResultsThe predictions for metabolic capacities of the symbionts in the host environment were in general agreement with previously reported genome analyses, each focused on the single-species level. The analysis suggests several previously un-reported routes for complementary interactions and estimated the dependency of each symbiont in specific host metabolites. No clear association was detected between metabolic co-dependencies and co-occurrence patterns.ConclusionsThe analysis generated predictions for testable hypotheses of metabolic exchanges and co-dependencies in bacterial communities and by crossing them with co-occurrence profiles, contextualized interaction patterns into a wider ecological perspective.

[1]  Shiri Freilich,et al.  Analysis of Microbial Functions in the Rhizosphere Using a Metabolic-Network Based Framework for Metagenomics Interpretation , 2017, Front. Microbiol..

[2]  M. Zimmermann,et al.  Transport in Plants I , 1975, Encyclopedia of Plant Physiology.

[3]  Roded Sharan,et al.  The large-scale organization of the bacterial network of ecological co-occurrence interactions , 2010, Nucleic acids research.

[4]  Kipp W. Johnson,et al.  Comparison of the Genome Sequences of “Candidatus Portiera aleyrodidarum” Primary Endosymbionts of the Whitefly Bemisia tabaci B and Q Biotypes , 2013, Applied and Environmental Microbiology.

[5]  N. Moran,et al.  Colloquium Papers: Symbiosis as an adaptive process and source of phenotypic complexity , 2007 .

[6]  A. Moya,et al.  Complete Genome Sequence of “Candidatus Portiera aleyrodidarum” BT-QVLC, an Obligate Symbiont That Supplies Amino Acids and Carotenoids to Bemisia tabaci , 2012, Journal of bacteriology.

[7]  Xiaowei Wang,et al.  Draft Genome Sequence of Rickettsia sp. Strain MEAM1, Isolated from the Whitefly Bemisia tabaci , 2012, Journal of bacteriology.

[8]  E. Rosenberg,et al.  Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. , 2008, FEMS microbiology reviews.

[9]  Z. Fei,et al.  Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects , 2015, Genome biology and evolution.

[10]  M. Ghanim,et al.  Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[11]  P. Buchner Endosymbiosis of Animals with Plant Microorganisms , 1965 .

[12]  S. Heuskin,et al.  Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies , 2011, Nature communications.

[13]  Bodil N. Cass,et al.  Cryptic diversity, reproductive isolation and cytoplasmic incompatibility in a classic biological control success story , 2016 .

[14]  Xiaoli Bing,et al.  Characterization of a Newly Discovered Symbiont of the Whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) , 2012, Applied and Environmental Microbiology.

[15]  J. Werren,et al.  Evolution and diversity of Rickettsia bacteria , 2009, BMC Biology.

[16]  Peter A. Robinson,et al.  Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework , 2010, PLoS Comput. Biol..

[17]  A. Moya,et al.  Two Host Clades, Two Bacterial Arsenals: Evolution through Gene Losses in Facultative Endosymbionts , 2015, Genome biology and evolution.

[18]  P. Baumann,et al.  Evolutionary Relationships of Primary Prokaryotic Endosymbionts of Whiteflies and Their Hosts , 2004, Applied and Environmental Microbiology.

[19]  Judith K. Brown Taxonomy, molecular systematics, and gene flow in the Bemisia tabaci complex and Bemisia relatives , 2010 .

[20]  Robert B. Waide,et al.  Developing and delivering scientific information in response to emerging needs , 2007 .

[21]  S. Andersson,et al.  Comparative Genomics of Wolbachia and the Bacterial Species Concept , 2013, PLoS genetics.

[22]  Adi Doron-Faigenboim,et al.  NetCmpt: a network-based tool for calculating the metabolic competition between bacterial species , 2012, Bioinform..

[23]  A. Moya,et al.  Learning how to live together: genomic insights into prokaryote–animal symbioses , 2008, Nature Reviews Genetics.

[24]  E. Vimr,et al.  Diversity of Microbial Sialic Acid Metabolism , 2004, Microbiology and Molecular Biology Reviews.

[25]  L. Boykin,et al.  Bemisia tabaci: a statement of species status. , 2011, Annual review of entomology.

[26]  Kostas Bourtzis,et al.  Manipulative tenants : bacteria associated with arthropods , 2011 .

[27]  K. V. van Wijk,et al.  Matching the supply of bacterial nutrients to the nutritional demand of the animal host , 2014, Proceedings of the Royal Society B: Biological Sciences.

[28]  J. Peretó,et al.  Nature lessons: the whitefly bacterial endosymbiont is a minimal amino acid factory with unusual energetics , 2016, bioRxiv.

[29]  Natalia N. Ivanova,et al.  GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes , 2010, Nature Methods.

[30]  Daniel B. Sloan,et al.  Endosymbiotic bacteria as a source of carotenoids in whiteflies , 2012, Biology Letters.

[31]  Orkun S. Soyer,et al.  Synthetic microbial communities , 2014, Current opinion in microbiology.

[32]  Honghe Sun,et al.  The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance , 2016, BMC Biology.

[33]  M. Ghanim,et al.  Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex , 2010, Molecular ecology.

[34]  O. Ebenhöh,et al.  The Metabolic Interplay between Plants and Phytopathogens , 2013, Metabolites.

[35]  D. Stahl,et al.  Metabolic modeling of a mutualistic microbial community , 2007, Molecular systems biology.

[36]  Roded Sharan,et al.  Competitive and cooperative metabolic interactions in bacterial communities. , 2011, Nature communications.

[37]  A. Aebi,et al.  Arthropod symbioses: a neglected parameter in pest- and disease-control programmes , 2011 .

[38]  A. Moya,et al.  Genome Evolution in the Primary Endosymbiont of Whiteflies Sheds Light on Their Divergence , 2015, Genome biology and evolution.

[39]  P. J. Boer The present status of the competitive exclusion principle. , 1986 .

[40]  A. Moya,et al.  The Genome of Cardinium cBtQ1 Provides Insights into Genome Reduction, Symbiont Motility, and Its Settlement in Bemisia tabaci , 2014, Genome biology and evolution.

[41]  Paul B. Rainey,et al.  Evolution of species interactions in a biofilm community , 2007, Nature.

[42]  Reinhart Heinrich,et al.  Structural analysis of expanding metabolic networks. , 2004, Genome informatics. International Conference on Genome Informatics.

[43]  Marie-France Sagot,et al.  Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci , 2015, BMC Genomics.

[44]  Daniel Segrè,et al.  Environments that Induce Synthetic Microbial Ecosystems , 2010, PLoS Comput. Biol..

[45]  L. Hersh,et al.  The Mitochondrial Peptidase Pitrilysin Degrades Islet Amyloid Polypeptide in Beta-Cells , 2015, PloS one.

[46]  Shiri Freilich,et al.  Variations in the identity and complexity of endosymbiont combinations in whitefly hosts , 2014, Front. Microbiol..

[47]  B. Py,et al.  Building Fe–S proteins: bacterial strategies , 2010, Nature Reviews Microbiology.

[48]  P. J. den Boer The present status of the competitive exclusion principle. , 1986, Trends in ecology & evolution.

[49]  A. Douglas,et al.  Cooperative Metabolism in a Three-Partner Insect-Bacterial Symbiosis Revealed by Metabolic Modeling , 2017, Journal of bacteriology.

[50]  Jean-Michel Claverie,et al.  Reductive Genome Evolution from the Mother of Rickettsia , 2007, PLoS genetics.

[51]  Parasitic wasp responses to symbiont-based defense in aphids , 2012, BMC Biology.

[52]  C. Marx Getting in Touch with Your Friends , 2009, Science.

[53]  N. Moran,et al.  Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole , 2015, Proceedings of the National Academy of Sciences.

[54]  G. Thomas,et al.  Genetic and metabolic determinants of nutritional phenotype in an insect–bacterial symbiosis , 2011, Molecular ecology.

[55]  Daniel Segrè,et al.  Ecosystems biology of microbial metabolism. , 2011, Current opinion in biotechnology.

[56]  I-Min A. Chen,et al.  IMG 4 version of the integrated microbial genomes comparative analysis system , 2013, Nucleic Acids Res..

[57]  Elhanan Borenstein,et al.  NetSeed: a network-based reverse-ecology tool for calculating the metabolic interface of an organism with its environment , 2012, Bioinform..

[58]  E. Borenstein,et al.  Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules , 2013, Proceedings of the National Academy of Sciences.

[59]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[60]  J. Hadfield,et al.  Horizontally Transmitted Symbionts and Host Colonization of Ecological Niches , 2013, Current Biology.

[61]  P. Silver,et al.  Emergent cooperation in microbial metabolism , 2010, Molecular systems biology.

[62]  M. Horn,et al.  Novel chlamydiae in whiteflies and scale insects: endosymbionts 'Candidatus Fritschea bemisiae' strain Falk and 'Candidatus Fritschea eriococci' strain Elm. , 2005, International journal of systematic and evolutionary microbiology.

[63]  J. Fuhrman General Distributions and the 'rare Biosphere' Microbial Community Structure and Its Functional Implications Review Insight , 2022 .

[64]  Connor T. Skennerton,et al.  CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes , 2015, Genome research.

[65]  Peer Bork,et al.  Metabolic dependencies drive species co-occurrence in diverse microbial communities , 2015, Proceedings of the National Academy of Sciences.

[66]  P. Baumann Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. , 2005, Annual review of microbiology.

[67]  P. Verma,et al.  Whitefly Genome Expression Reveals Host-Symbiont Interaction in Amino Acid Biosynthesis , 2015, PloS one.

[68]  F. Nardi,et al.  Members of Bemisia tabaci (Hemiptera: Aleyrodidae) Cryptic Species and the Status of Two Invasive Alien Species in the Yunnan Province (China) , 2014, Journal of insect science.

[69]  J. Jaenike Population genetics of beneficial heritable symbionts. , 2012, Trends in ecology & evolution.

[70]  J. McCutcheon,et al.  An Interdependent Metabolic Patchwork in the Nested Symbiosis of Mealybugs , 2011, Current Biology.

[71]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[72]  Wolfgang Wiechert,et al.  Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms , 2012, Microbial Cell Factories.

[73]  R. Overbeek,et al.  Missing genes in metabolic pathways: a comparative genomics approach. , 2003, Current opinion in chemical biology.

[74]  J. Stuart,et al.  Journal of Insect Science: Vol. 2006 | Article 12 , 2006 .

[75]  M. Mescher,et al.  Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. , 2012, Insect biochemistry and molecular biology.

[76]  A. Himler,et al.  Rapid Spread of a Bacterial Symbiont in an Invasive Whitefly Is Driven by Fitness Benefits and Female Bias , 2011, Science.