Abstract
Air pollution has a deleterious impact on public health and the environment. There is few knowledge on the effect of air pollution on terrestrial microbial communities, despite the major role of microbes in ecosystems. Here, we designed an in situ trial ecosystem to assess the impact of moderate atmospheric pollution, below World Health Organization (WHO) thresholds, on an indigenous microbial communities, including bacteria, fungi, ciliates, algae, cyanobacteria, testate amoebae, rotifers and nematodes, extracted from terrestrial bryophytes. These micro-ecosystems were placed at a rural, an urban and an industrial site in France and were thus exposed to various levels of nitrogen dioxide (NO2), from 6.6–67.9 μg·m−3, and particulate matter, from 0.7–7.9 μg·m−3. Microbial analysis was performed by microscopy. We determined atmospheric temperature, relative humidity and particulate matter with diameter lower than 10 µm (PM10), Cu, Cr, Fe, Ni, Pb, Zn in PM10, and (NO2). Results show a significant impact of chronic moderate exposure to NO2 and copper Cu-associated particulate matter on the global microbial network complexity. This is evidenced by a loss of about 40 % of microbial co-occurrence links during incubation. Most lost microbial links are ecologically positive links. Moreover, most changes in community co-occurrence networks are related to testate amoebae, a major top predator of microbes. Overall, our findings demonstrate that air pollution can have strong deleterious effects on microbial interactions, even at levels below WHO thresholds.
Similar content being viewed by others
References
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5(May):219
Blouin M, Karimi B, Mathieu J, Lerch TZ (2015) Levels and limits in artificial selection of communities. Ecol Lett 18(10):1040–1048
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162(3):617–631
Burns TP, Rose KA, Brenkert AL (2014) Quantifying direct and indirect effects of perturbations using model ecosystems. Ecol Model 293:69–80
Chodak M, Gołebiewski M, Morawska-Płoskonka J, Kuduk K, Niklinsk M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14
El-Sheekh MM, El-Shouny W, Osman MEH, El-Gammal EWE (2005) Growth and heavy metals removal efficiency of Nostoc muscorum and Anabaena subcylindrica in sewage and industrial wastewater effluents. Environ Toxicol Pharmacol 19(2):357–365
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10(8):538–550
Fernández-Luqueño F, Valenzuela-encinas C, Marsch R, Martinez-Suarez C, Vasquez-Nunez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil-possibilities and challenges: a review. Environ Sci Pollut Res 18(1):12–30
Gaudry A, Moskura M, Mariet C, Ayrault S, Denayer F, Bernard N (2008) Inorganic pollution in PM10 particles collected over three French sites under various influences: rural conditions, traffic and industry. Water Air Soil Pollut 193(1–4):91–106
Gilbert D, Amblard C, Bourdier G, Francez AJ (1998) The microbial loop at the surface of a peatland: structure, function, and impact of nutrient input. Microb Ecol 35:83–93
Gurjar BR, Molina LT, Ojha CSP (2010) Air pollution: health and environmental impacts. CRC press
Han X, Naeher LP (2006) A review of traffic-related air pollution exposure assessment studies in the developing world. Environ Int 32(1):106–120
Jassey VEJ, Meyer C, Dupuy C, Bernard N, Mitchell EAD, Toussaint ML, Metian M, Chatelain AP, Gilbert D (2013) To what extent do food preferences explain the trophic position of heterotrophic and mixotrophic microbial consumers in a Sphagnum peatland? Microb Ecol 66(3):571–580. doi:10.1007/s00248-013-0262-8
Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer, Berlin
Levin SA (1998) Ecosystems and the biosphere as complex adaptive systems. Ecosystems 431–436
Lovett GM, Tear TH, Evers DC, Findlay SEG et al (2009) Effects of air pollution on ecosystems and biological diversity in the eastern United States. Ann N Y Acad Sci 1162:99–135. doi:10.1111/j.1749-6632.2009.04153.x
McFrederick QS, Fuentes JD, Rouston T, Kathilankal JC, Lerdau M (2009) Effects of air pollution on biogenic volatiles and ecological interactions. Oecologia 160(3):411–420
Meyer C, Gilbert D, Gaudry A, Franchi M, Nguyen-Viet H, Fabure J, Bernard N (2010) Relationship of atmospheric pollution characterized by gas (NO2) and particles (PM10) to microbial communities living in bryophytes at three differently polluted sites (rural, urban, and industrial). Environ Microbiol 59(2):324–334
Meyer C, Gillet F, Moskura M, Franchi M, Bernard N (2012) Using “bryophytes and their associated testate amoeba” microsystems as indicators of atmospheric pollution. Ecol Indic 13(1):144–151. doi:10.1016/j.ecolind.2011.05.020
Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442(7100):259–264
Mougi A, Kondoh M (2014) Stability of competition-antagonism-mutualism hybrid community and the role of community network structure. J Theor Biol 360:54–58
Nguyen-Viet H, Gilbert D, Mitchell EAD, Badot P, Bernard N (2008) Effects of experimental lead pollution on the microbial communities associated with Sphagnum fallax (Bryophyta). Microb Ecol. doi:10.1007/s00248-006-9192-z
Paine RT (1966) Food web complexity and species diversity. Am Nat 100(910):65–75
Palmes E, Gunnison AF, DiMattio J, Tomczik C (1976) Personal sampler for nitrogen dioxide. Am Ind Hyg Assoc J 37(10):570–577. doi:10.1080/0002889768507522
Ricklefs RE, Miller GL (2005) Ecology, 4th edn. D. B. & Larcier ed
Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J 3(6):675–684. doi:10.1038/ismej.2009.11
Sauve AMC, Fontaine C, Thébault E (2014) Structure-stability relationships in networks combining mutualistic and antagonistic interactions. Oikos 123(3):378–384
Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualisic and trophic networks. Science 329:853–856
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11(12):1351–1363. doi:10.1111/j.1461-0248.2008.01250.x
Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143(10):2270–2279. doi:10.1016/j.biocon.2009.12.004
Widder S, Besemer K, Singer GA, Ceola S, Bertuzzo E, Quince C et al (2014) Fluvial network organization imprints on microbial co-occurrence networks. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1411723111
Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol 23(11):596–599
Zappelini C, Karimi B, Foulon J, Lacercat-Didier L, Maillard F, Valot B, Blaudez D, Cazaux D, Gilbert D, Yergeau E, Greer C, Chalot M (2015) Diversity and complexity of microbial communities from a chlor-alkali tailings dump. Soil Biol Biochem 90:101–110. doi:10.1016/j.soilbio.2015.08.008
Acknowledgments
This research is a component of the µPOLAIR project, which focuses on Sphagnum peatlands to quantify the long-range deposition of atmospheric pollutants and evaluate their impact on the environment. The µPOLAIR project is supported by the PRIMEQUAL programme (French Ministry of the Environment and the Agence De l’Environnement et de la Maitrise de l’Energie; Grant Number 2010-Q.3-Chorus2100082984) and the city of Besançon (France). B.K. received a Ph.D. grant from the French Ministry of Higher Education and Research. The authors would like to thank the staff of the CEA of Saclay for their collaboration in analyses of the trace elements. The authors also would like to thank Lionel Ranjard for suggestions on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Battle Karimi and Caroline Meyer have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Karimi, B., Meyer, C., Gilbert, D. et al. Air pollution below WHO levels decreases by 40 % the links of terrestrial microbial networks. Environ Chem Lett 14, 467–475 (2016). https://doi.org/10.1007/s10311-016-0589-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10311-016-0589-8