Linking the development and functioning of a carnivorous pitcher plant’s microbial digestive community

Ecosystem development theory predicts that successional turnover in community composition can influence ecosystem functioning. However, tests of this theory in natural systems are made difficult by a lack of replicable and tractable model systems. Using the microbial digestive associates of a carnivorous pitcher plant, I tested hypotheses linking host age-driven microbial community development to host functioning. Monitoring the yearlong development of independent microbial digestive communities in two pitcher plant populations revealed a number of trends in community succession matching theoretical predictions. These included mid-successional peaks in bacterial diversity and metabolic substrate use, predictable and parallel successional trajectories among microbial communities, and convergence giving way to divergence in community composition and carbon substrate use. Bacterial composition, biomass, and diversity positively influenced the rate of prey decomposition, which was in turn positively associated with a host leaf’s nitrogen uptake efficiency. Overall digestive performance was greatest during late summer. These results highlight links between community succession and ecosystem functioning and extend succession theory to host-associated microbial communities.

[1]  C. Violle,et al.  Decreases in average bacterial community rRNA operon copy number during succession , 2015, The ISME Journal.

[2]  Michel Loreau,et al.  Ecosystem development explained by competition within and between material cycles , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  Jesse R. Zaneveld,et al.  Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences , 2013, Nature Biotechnology.

[4]  Simeone Marino,et al.  Mathematical modeling of primary succession of murine intestinal microbiota , 2013, Proceedings of the National Academy of Sciences.

[5]  E. Odum.  The strategy of ecosystem development. , 1969, Science.

[6]  O. Loucks,et al.  Evolution of diversity, efficiency, and community stability. , 1970, American zoologist.

[7]  M. Bradford,et al.  Testing the functional significance of microbial community composition. , 2009, Ecology.

[8]  T. Schmidt,et al.  rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria , 2000, Applied and Environmental Microbiology.

[9]  S. Reed,et al.  Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. , 2007, Ecology.

[10]  A. Agresti,et al.  Categorical Data Analysis , 1991, International Encyclopedia of Statistical Science.

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

[12]  ECOSYSTEM SUCCESSION, NUTRIENT CYCLING AND OUTPUT INPUT RATIOS , 1982 .

[13]  Minoru Kanehisa,et al.  KEGG as a reference resource for gene and protein annotation , 2015, Nucleic Acids Res..

[14]  J. Connell,et al.  Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization , 1977, The American Naturalist.

[15]  W. Whitman,et al.  Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons , 2013 .

[16]  F. Chapin,et al.  EFFECTS OF BIODIVERSITY ON ECOSYSTEM FUNCTIONING: A CONSENSUS OF CURRENT KNOWLEDGE , 2005 .

[17]  James P. Grover,et al.  Dynamics of Nutrient Cycling and Food Webs , 1992 .

[18]  Josu G. Alday,et al.  Vegetation convergence during early succession on coal wastes: a 6-year permanent plot study , 2011 .

[19]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[20]  B. Lugtenberg,et al.  Plant-growth-promoting rhizobacteria. , 2009, Annual review of microbiology.

[21]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[22]  A. Ellison,et al.  Linking the brown and green: nutrient transformation and fate in the Sarracenia microecosystem. , 2008, Ecology.

[23]  Nancy B. Grimm,et al.  TEMPORAL SUCCESSION IN A DESERT STREAM ECOSYSTEM FOLLOWING FLASH FLOODING , 1982 .

[24]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[25]  Norman L. Christensen,et al.  Secondary Forest Succession on the North Carolina Piedmont , 1981 .

[26]  John C. Tan,et al.  Freshwater bacterial lifestyles inferred from comparative genomics. , 2014, Environmental microbiology.

[27]  S. Pickett,et al.  An Integrative Approach to Successional Dynamics: Tempo and Mode of Vegetation Change , 2015 .

[28]  S. Allison,et al.  Effects of dispersal and selection on stochastic assembly in microbial communities , 2016, The ISME Journal.

[29]  Yan Mei,et al.  The RNA-binding protein hnRNPLL induces a T cell alternative splicing program delineated by differential intron retention in polyadenylated RNA , 2014, Genome Biology.

[30]  Michel Loreau,et al.  Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  Johan van de Koppel,et al.  Reconciling complexity with stability in naturally assembling food webs , 2007, Nature.

[32]  R. Parthasarathy,et al.  Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut , 2014, mBio.

[33]  Jonathan M. Chase,et al.  Evolutionary diversification in stickleback affects ecosystem functioning , 2009, Nature.

[34]  Mary K. Firestone,et al.  Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest , 2005 .

[35]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[36]  Ian T. Carroll,et al.  Impacts of plant diversity on biomass production increase through time because of species complementarity , 2007, Proceedings of the National Academy of Sciences.

[37]  R. Amann,et al.  Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom , 2012, Science.

[38]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[39]  Matthew J. Gebert,et al.  Microbial community assembly and metabolic function during mammalian corpse decomposition , 2016, Science.

[40]  Johan van de Koppel,et al.  Reconciling complexity with stability in naturally assembling food webs , 2009, Nature.

[41]  S. Hättenschwiler,et al.  Functional diversity of terrestrial microbial decomposers and their substrates. , 2011, Comptes rendus biologies.

[42]  F. Berendse,et al.  Diversity-productivity relationships: initial effects, long-term patterns, and underlying mechanisms. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  John Pastor,et al.  Dynamics of nutrient cycling and food webs , 1992 .

[44]  Norman L. Christensen,et al.  CONVERGENCE DURING SECONDARY FOREST SUCCESSION , 1984 .

[45]  A. Ives,et al.  Effects of species diversity on community biomass production change over the course of succession. , 2007, Ecology.

[46]  R. Knight,et al.  Changes through time: integrating microorganisms into the study of succession. , 2010, Research in microbiology.

[47]  M. Willig,et al.  Succession of Macroinvertebrates in Playas of the Southern High Plains, USA , 1998, Journal of the North American Benthological Society.

[48]  Peter M. Vitousek,et al.  Ecosystem Succession and Nutrient Retention: A Hypothesis , 1975 .

[49]  Davey L. Jones,et al.  Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? , 2016, Front. Microbiol..

[50]  Thomas M. Smith,et al.  Plant Succession: Life History and Competition , 1987, The American Naturalist.

[51]  S. Scheu,et al.  Niche dimensionality links biodiversity and invasibility of microbial communities , 2013 .

[52]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[53]  F. Bäckhed,et al.  Host-Bacterial Mutualism in the Human Intestine , 2005, Science.

[54]  J. Neu,et al.  Succession of microbial consortia in the developing infant gut microbiome , 2011 .

[55]  David W. Armitage.  Time-variant species pools shape competitive dynamics and biodiversity–ecosystem function relationships , 2016, Proceedings of the Royal Society B: Biological Sciences.

[56]  Daniel B. DiGiulio,et al.  Development of the Human Infant Intestinal Microbiota , 2007, PLoS biology.

[57]  Alan Agresti,et al.  Categorical Data Analysis, 3rd Edition Extra Exercises , 2012 .

[58]  D. Wall,et al.  Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships , 2011 .

[59]  Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities , 2012, Oecologia.

[60]  N. Fierer,et al.  Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics , 2009, Microbial Ecology.

[61]  P. Rainey,et al.  Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris) , 1993, Plant and Soil.

[62]  John L. Orrock,et al.  Local community size mediates ecological drift and competition in metacommunities , 2010, Proceedings of the Royal Society B: Biological Sciences.

[63]  D. Tilman.  Constraints and tradeoffs: toward a predictive theory of competition and succession , 1990 .

[64]  J. V. van Elsas,et al.  Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession , 2015, Proceedings of the National Academy of Sciences.

[65]  R. A. Beaver,et al.  Geographical variation in food web structure in Nepenthes pitcher plants , 1985 .

[66]  B. Silverman,et al.  The contribution of species richness and composition to bacterial services , 2005, Nature.

[67]  Mark Vellend,et al.  The Theory of Ecological Communities (Mpb-57) , 2016 .

[68]  L. Wolfe.  Feeding Behavior of a Plant: Differential Prey Capture in Old and New Leaves of the Pitcher Plant (Sarracenia purpurea) , 1981 .

[69]  Mehdi Layeghifard,et al.  Seasonal community succession of the phyllosphere microbiome. , 2015, Molecular plant-microbe interactions : MPMI.

[70]  A. Arkin,et al.  Stochasticity, succession, and environmental perturbations in a fluidic ecosystem , 2014, Proceedings of the National Academy of Sciences.

[71]  A. Auclair,et al.  Diversity Relations of Upland Forests in the Western Great Lakes Area , 1971, The American Naturalist.