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Insect-associated bacterial communities in an alpine stream

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Abstract

The roles of macroinvertebrate and microbial communities in stream ecosystems are recognized to be important to energy flow and nutrient cycling. While the linkages of these major groups of aquatic organisms have not been thoroughly investigated, determining how they interact is particularly important for understanding the mechanisms and potential evolutionary relationships that contribute to ecosystem processes, such as organic matter decomposition. We evaluated the microbiomes of several aquatic insect species differing in trophic ecology and belonging to different functional feeding groups at two sites along an Italian Alpine river with different elevation and environmental characteristics, one located above the tree line and the other in a forested environment. We found that the internal microbial communities of the different species significantly varied in taxonomic and functional composition and could be used to classify samples to both species and environment. We demonstrated that functional differences existed between the microbiota of different insect species with variable feeding behaviors, and that species differences were more important, in this context, than environmental or habitat conditions. These results provide new information on how the microbiomes of aquatic insects may potentially be influenced by their hosts and habitat conditions in Alpine streams.

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References

  • Alonso-Pernas, P., S. Bartram, E. M. Arias-Cordero, A. L. Novoselov, L. Halty-deLeon, Y. Shao & W. Boland, 2017. In vivo isotopic labeling of symbiotic bacteria involved in cellulose degradation and nitrogen recycling within the gut of the Forest Cockchafer (Melolontha hippocastani). Frontiers in Microbiology 8: 1970.

    PubMed  PubMed Central  Google Scholar 

  • Alonso-Pernas, P., S. Bartram, E. M. Arias-Cordero, A. L. Novoselov, L. Halty-deLeon, Y. Shao & W. Boland, 2018. Corrigendum: in vivo isotopic labeling of symbiotic bacteria involved in cellulose degradation and nitrogen recycling within the gut of the forest Cockchafer (Melolontha hippocastani). Frontiers in Microbiology 9: 488.

    PubMed  PubMed Central  Google Scholar 

  • Anderson, N. & A. Cargill, 1987. Nutritional ecology of aquatic detritivorous insects. In Slansky, F. (ed.), Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. Wiley, New York: 903–925.

    Google Scholar 

  • APAT-IRSA, 2003. Metodi analitici per le acque. Manuali e linee Guida 29: 1149.

    Google Scholar 

  • Ayayee, P. A., C. R. Cosgrove, A. Beckwith, A. A. Roberto & L. G. Leff, 2018. Gut bacterial assemblages of freshwater macroinvertebrate functional feeding groups. Hydrobiologia 822: 157–172.

    CAS  Google Scholar 

  • Baldy, V., M. O. Gessner & E. Chauvet, 1995. Bacteria, fungi and the breakdown of leaf litter in a large river. Oikos 74(1): 93–102.

    Google Scholar 

  • Belfiore, C., 1983. Ephemeroptera: Guide per il riconoscimento delle specie animali delle acque interne italiane. Consiglio Nazionale delle Ricerche AQ/1/201:113.

  • Benbow, M. E., J. L. Pechal & A. K. Ward, 2017. Heterotrophic bacteria production and microbial community assessment. In Hauer, F. R. & G. A. Lamberti (eds), Methods in Stream Ecology: Volume 1: Ecosystem Structure, 3rd ed. Elsevier, Cambridge: 161–176.

    Google Scholar 

  • Benbow, M. E., P. S. Barton, M. D. Ulyshen, J. C. Beasley, T. L. DeVault, M. S. Strickland, J. K. Tomberlin, H. R. Jordan & J. L. Pechal, 2019. Necrobiome framework for bridging decomposition ecology of autotrophically and heterotrophically derived organic matter. Ecological Monographs. https://doi.org/10.1002/ecm.1331.

    Article  Google Scholar 

  • Besemer, K., G. Singer, C. Quince, E. Bertuzzo, W. Sloan & T. J. Battin, 2013. Headwaters are critical reservoirs of microbial diversity for fluvial networks. Proceedings of the Royal Society B: Biological Sciences 280: 20131760.

    PubMed  Google Scholar 

  • Bokulich, N. A., B. D. Kaehler, J. R. Rideout, M. Dillon, E. Bolyen, R. Knight, G. A. Huttley & J. G. Caporaso, 2018. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6: 90.

    PubMed  PubMed Central  Google Scholar 

  • Bolyen, E., J. R. Rideout, M. R. Dillon, N. A. Bokulich, C. Abnet, G. A. Al-Ghalith, H. Alexander, E. J. Alm, M. Arumugam & F. Asnicar, 2018. QIIME 2: reproducible, interactive, scalable, and extensible microbiome data science. PeerJ Preprints 6: e27295v2.

    Google Scholar 

  • Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. A. Johnson & S. P. Holmes, 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13: 581.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso, J. G., C. L. Lauber, W. A. Walters, D. Berg-Lyons, C. A. Lozupone, P. J. Turnbaugh, N. Fierer & R. Knight, 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences 108: 4516–4522.

    CAS  Google Scholar 

  • Claesson, M. J., S. Cusack, O. O’Sullivan, R. Greene-Diniz, H. de Weerd, E. Flannery, J. R. Marchesi, D. Falush, T. Dinan, G. Fitzgerald, C. Stanton, D. van Sinderen, M. O’Connor, N. Harnedy, K. O’Connor, C. Henry, D. O’Mahony, A. P. Fitzgerald, F. Shanahan, C. Twomey, C. Hill, R. P. Ross & P. W. O’Toole, 2010. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proceedings of the National Academy of Sciences USA 108: 4586–4591.

    Google Scholar 

  • Cummins, K. W., 1974. Structure and function of stream ecosystems. Bioscience 24: 631–641.

    Google Scholar 

  • Cummins, K. W., 2016. Combining taxonomy and function in the study of stream macroinvertebrates. Journal of Limnology 75: 235–241.

    Google Scholar 

  • Cummins, K. W. & M. J. Klug, 1979. Feeding ecology of stream invertebrates. Annual Review of Ecology and Systematics 10: 147–172.

    Google Scholar 

  • Cummins, K. W., R. C. Petersen, F. O. Howard, J. C. Wuycheck & V. I. Holt, 1973. The utilization of leaf litter by stream detritivores. Ecology 54: 336–345.

    Google Scholar 

  • Danger, M., J. Cornut, E. Chauvet, P. Chavez, A. Elger & A. Lecerf, 2013. Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect? Ecology 94: 1604–1613.

    PubMed  Google Scholar 

  • Doretto, A., F. Bona, E. Falasco, E. Piano, P. Tizzani & S. Fenoglio, 2016. Fine sedimentation affects CPOM availability and shredder abundance in Alpine streams. Journal of Freshwater Ecology 31: 299–302.

    CAS  Google Scholar 

  • Doretto, A., F. Bona, E. Piano, I. Zanin, A. C. Eandi & S. Fenoglio, 2017. Trophic availability buffers the detrimental effects of clogging in an alpine stream. Science of the Total Environment 592: 503–511.

    CAS  PubMed  Google Scholar 

  • Douglas, A. E., 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology 60: 17–34.

    CAS  PubMed  Google Scholar 

  • Eggert, S. & J. Wallace, 2007. Wood biofilm as a food resource for stream detritivores. Limnology and Oceanography 52: 1239–1245.

    Google Scholar 

  • Faith, D. P. & A. M. Baker, 2006. Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges. Evolutionary Bioinformatics 2: 117693430600200007.

    Google Scholar 

  • Falasco, E. & F. Bona, 2011. Diatom community biodiversity in an Alpine protected area: a study in the Maritime Alps Natural Park. Journal of Limnology 70: 157–167.

    Google Scholar 

  • Fenoglio, S., T. Bo, M. Cammarata, M. J. López-Rodríguez & J. M. Tierno de Figueroa, 2015. Seasonal variation of allochthonous and autochthonous energy inputs in an alpine stream. Journal of Limnology 74(2): 272–277.

    Google Scholar 

  • Fochetti, R. & J. M. Tiernod e Figueroa, 2008. Plecoptera. In Calderini, (ed.), Fauna d’Italia, Vol. XLIII. NHBS, London: 350.

    Google Scholar 

  • Golladay, S. W., 1997. Suspended particulate organic matter concentration and export in streams. Journal of the North American Benthological Society 16: 122–131.

    Google Scholar 

  • Gupta, P., K. Samant & A. Sahu, 2012. Isolation of cellulose-degrading bacteria and determination of their cellulolytic potential. International Journal of Microbiology 2012: 5.

    Google Scholar 

  • Henry, L. M., M. C. Maiden, J. Ferrari & H. C. J. Godfray, 2015. Insect life history and the evolution of bacterial mutualism. Ecology Letters 18: 516–525.

    PubMed  Google Scholar 

  • Hieber, M., C. T. Robinson, U. Uehlinger & J. Ward, 2005. A comparison of benthic macroinvertebrate assemblages among different types of alpine streams. Freshwater Biology 50: 2087–2100.

    Google Scholar 

  • Hocking, M. D. & T. E. Reimchen, 2006. Consumption and distribution of salmon (Oncorhynchus spp.) nutrients and energy by terrestrial flies. Canadian Journal of Fisheries and Aquatic Science 63: 2076–2086.

    Google Scholar 

  • Hooper, L. V., D. R. Littman & A. J. Macpherson, 2012. Interactions between the microbiota and the immune system. Science 336: 1268–1273.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Junk, W. J., P. B. Bayley & R. E. Sparks, 1989. The flood pulse concept in river-floodplain systems. Canadian Special Publication in Fisheries and Aquatic Science 106: 110.

    Google Scholar 

  • Kassambara, A., 2017. ggpubr:“ggplot2” based publication ready plots. R Package Version 01: 6.

    Google Scholar 

  • Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaufman, M. G., E. D. Walker, D. A. Odelson & M. J. Klug, 2000. Microbial community ecology & insect nutrition. American Entomologist 46: 173–185.

    Google Scholar 

  • Klug, M. & S. Kotarski, 1980. Bacteria associated with the gut tract of larval stages of the aquatic cranefly Tipula abdominalis (Diptera; Tipulidae). Applied Environmental Microbiology 40: 408–416.

    CAS  PubMed  Google Scholar 

  • Kozich, J. J., S. L. Westcott, N. T. Baxter, S. K. Highlander & P. D. Schloss, 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied Environmental Microbiology 79: 5112–5120.

    CAS  PubMed  Google Scholar 

  • Kuehn, K. A., 2016. Lentic and lotic habitats as templets for fungal communities: traits, adaptations, and their significance to litter decomposition within freshwater ecosystems. Fungal Ecology 19: 135–154.

    Google Scholar 

  • Langille, M. G., 2018. Exploring linkages between taxonomic and functional profiles of the human microbiome. MSystems 3: e00163.

    PubMed  PubMed Central  Google Scholar 

  • Langille, M. G., J. Zaneveld, J. G. Caporaso, D. McDonald, D. Knights, J. A. Reyes, J. C. Clemente, D. E. Burkepile, R. L. V. Thurber, R. Knight, R. G. Beiko & C. Huttenhower, 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31: 814–821.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen, T., M. Ventura, K. Maraldo, X. Triadó-Margarit, E. O. Casamayor, Y. V. Wang, N. Andersen & D. M. O’brien, 2016. The dominant detritus-feeding invertebrate in Arctic peat soils derives its essential amino acids from gut symbionts. Journal of Animal Ecology 85: 1275–1285.

    PubMed  Google Scholar 

  • Lawson, D. L. & M. J. Klug, 1989. Microbial fermentation in the hindguts of two stream detritivores. Journal of the North American Benthological Society 8: 85–91.

    Google Scholar 

  • Lawson, D. L., M. J. Klug & R. W. Merritt, 1984. The influence of the physical, chemical, and microbiological characteristics of decomposing leaves on the growth of the detritivore Tipula abdominalis (Diptera: Tipulidae). Canadian Journal of Zoology 62: 2339–2343.

    Google Scholar 

  • Liaw, A. & M. Wiener, 2002. Classification and regression by randomForest. R news 2: 18–22.

    Google Scholar 

  • Louca, S. & M. Doebeli, 2017. Efficient comparative phylogenetics on large trees. Bioinformatics 34: 1053–1055.

    Google Scholar 

  • Mason, C. J., E. D. Scully, S. M. Geib & K. Hoover, 2016. Contrasting diets reveal metabolic plasticity in the tree-killing beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae). Scientific Reports 6: 33813.

    CAS  PubMed  PubMed Central  Google Scholar 

  • McMurdie, P. J. & S. Holmes, 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8: e61217.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merritt, R. W. & K. W. Cummins, 2006. Trophic relationships of macroinvertebrates. In Hauer, F. R. & G. A. Lamberti (eds), Methods in Stream Ecology. Academic Press, New York: 585–609.

    Google Scholar 

  • Moore, J. C., E. L. Berlow, D. C. Coleman, P. C. de Ruiter, Q. Dong, A. Hastings, N. C. Johnson, K. S. McCann, K. Melville, P. J. Morin, K. Nadelhoffer, A. D. Rosemond, D. M. Post, J. L. Sabo, K. M. Scow, M. J. Vanni & D. H. Wall, 2004. Detritus, trophic dynamics and biodiversity. Ecology Letters 7: 584–600.

    Google Scholar 

  • Moran, N. A. & A. Telang, 1998. Bacteriocyte-associated symbionts of insects. Bioscience 48: 295–304.

    Google Scholar 

  • Moretti, G., 1983. Tricotteri. Guide per il riconoscimento delle specie animali delle acque interne italiane. Consiglio Nazionale delle Ricerche AQ/1/196:155.

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, B. O’hara, G. L. Simpson, P. Solymos, M. H. Stevens & H. Wagner, 2015. Package ‘vegan’. Community Ecology Package, Version 2(9): 1–295.

    Google Scholar 

  • Pechal, J. L. & M. E. Benbow, 2016. Microbial ecology of the salmon necrobiome: evidence salmon carrion decomposition influences aquatic and terrestrial insect microbiomes. Environmental Microbiology 18: 1511–1522.

    CAS  PubMed  Google Scholar 

  • Pechal, J. L., T. L. Crippen, A. M. Tarone, A. J. Lewis, J. K. Tomberlin & M. E. Benbow, 2013. Microbial community functional change during vertebrate carrion decomposition. PLoS ONE 8: e79035.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pechal, J. L., T. L. Crippen, J. A. Cammack, J. K. Tomberlin & M. E. Benbow, 2019. Microbial communities of salmon resource subsidies and associated necrophagous consumers during decomposition: potential of cross-ecosystem microbial dispersal. Food Webs 19: e00114.

    Google Scholar 

  • Price, M. N., P. S. Dehal & A. P. Arkin, 2010. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490.

    PubMed  PubMed Central  Google Scholar 

  • R core development team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Radivojac, P., W. T. Clark, T. R. Oron, A. M. Schnoes, T. Wittkop, A. Sokolov, K. Graim, C. Funk, K. Verspoor & A. Ben-Hur, 2013. A large-scale evaluation of computational protein function prediction. Nature Methods 10: 221.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Receveur, J. P., J. L. Pechal, M. E. Benbow, G. Donato, T. Rainey & J. R. Wallace, 2018. Changes in larval mosquito microbiota reveal non-target effects of insecticide treatments in hurricane-created habitats. Microbial Ecology. https://doi.org/10.1007/s00248-018-1175-3.

    Article  PubMed  Google Scholar 

  • Ridley, E. V., A. C. N. Wong, S. Westmiller & A. E. Douglas, 2012. Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS ONE 7: e36765.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivosecchi, L., 1984. Ditteri (Diptera): guide per il riconoscimento delle specie animali delle acque interne italiane. Consiglio Nazionale delle Ricerche AQ 1: 28.

    Google Scholar 

  • Rosenfeld, J. S., 2002. Functional redundancy in ecology and conservation. Oikos 98: 156–162.

    Google Scholar 

  • Russell, J. A., C. S. Moreau, B. Goldman-Huertas, M. Fujiwara, D. J. Lohman & N. E. Pierce, 2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proceedings of the National Academy of Sciences 106: 21236–21241.

    CAS  Google Scholar 

  • Savio, D., L. Sinclair, U. Z. Ijaz, J. Parajka, G. H. Reischer, P. Stadler, A. P. Blaschke, G. Blöschl, R. L. Mach & A. K. Kirschner, 2015. Bacterial diversity along a 2600 km river continuum. Environmental Microbiology 17: 4994–5007.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sedell, J. R., J. E. Richey & F. J. Swanson, The river continuum concept: a basis for the expected ecosystem behavior of very large rivers. In: Proceedings of the international large river symposium, 1989. vol 106. Canadian Special Publication of Fisheries and Aquatic Sciences, p 49–55.

  • Statzner, B. & B. Higler, 1985. Questions and comments on the river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 42: 1038–1044.

    Google Scholar 

  • Steffan, S. A. & P. S. Dharampal, 2018. Undead food-webs: Integrating microbes into the food-chain. Food Webs 16: e00111.

    Google Scholar 

  • Straka, M., V. Syrovátka & J. Helešic, 2012. Temporal and spatial macroinvertebrate variance compared: crucial role of CPOM in a headwater stream. Hydrobiologia 686: 119–134.

    Google Scholar 

  • Tank, J. L., E. J. Rosi-Marshall, N. A. Griffiths, S. A. Entrekin & M. L. Stephen, 2010. A review of allochthonous organic matter dynamics and metabolism in streams. Journal of the North American Benthological Society 29: 118–146.

    Google Scholar 

  • Vannote, R. L., G. W. Minshall, K. W. Cummins, J. R. Sedell & C. E. Cushing, 1980. River continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37: 130–137.

    Google Scholar 

  • Wagner, K., K. Besemer, N. R. Burns, T. J. Battin & M. M. Bengtsson, 2015. Light availability affects stream biofilm bacterial community composition and function, but not diversity. Environmental Microbiology 17: 5036–5047.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ward, D. & D. Saltz, 1994. Foraging at different spatial scales: Dorcas Gazelles foraging for lilies in the Negev Desert. Ecology 75: 48–58.

    Google Scholar 

  • Ward, J. V. & J. A. Stanford, 1995. The serial discontinuity concept: extending the model to floodplain rivers. Regulated Rivers: Research & Management 10: 159–168.

    Google Scholar 

  • Weatherbee, C., J. Pechal & M. Benbow, 2017. The dynamic maggot mass microbiome. Annals of the Entomological Society of America 110: 45–53.

    Google Scholar 

  • Webster, J. & E. Benfield, 1986. Vascular plant breakdown in freshwater ecosystems. Annual Review of Ecology and Systematics 17: 567–594.

    Google Scholar 

  • Wickham, H., 2016. ggplot2: elegant graphics for data analysis. Springer, New York.

    Google Scholar 

  • Widder, S., K. Besemer, G. A. Singer, S. Ceola, E. Bertuzzo, C. Quince, W. T. Sloan, A. Rinaldo & T. J. Battin, 2014. Fluvial network organization imprints on microbial co-occurrence networks. Proceedings of the National Academy of Sciences 111: 12799–12804.

    CAS  Google Scholar 

  • Wilhelm, L., K. Besemer, L. Fragner, H. Peter, W. Weckwerth & T. J. Battin, 2015. Altitudinal patterns of diversity and functional traits of metabolically active microorganisms in stream biofilms. The ISME Journal 9: 2454.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winterbourn, M. J., J. Rounick & B. Cowie, 1981. Are New Zealand stream ecosystems really different? New Zealand Journal of Marine and Freshwater Research 15: 321–328.

    Google Scholar 

  • Yun, J.-H., S. W. Roh, T. W. Whon, M.-J. Jung, M.-S. Kim, D.-S. Park, C. Yoon, Y.-D. Nam, Y.-J. Kim & J.-H. Choi, 2014. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied Environmental Microbiology 80: 5254–5264.

    PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Courtney Weatherbee for assistance in processing insect specimens as well as the anonymous reviewers whose thoughtful comments greatly improved the manuscript.

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Partial funding was provided by the College of Agriculture and Natural Resources, the Department of Entomology and AgBioResearch at Michigan State University.

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Correspondence to M. Eric Benbow.

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Receveur, J.P., Fenoglio, S. & Benbow, M.E. Insect-associated bacterial communities in an alpine stream. Hydrobiologia 847, 331–344 (2020). https://doi.org/10.1007/s10750-019-04097-w

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