Analysis of interdomain taxonomic patterns in urban street mats.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Author(s): Hervé V;Hervé V; Lopez PJ; Lopez PJ
  • Source:
    Environmental microbiology [Environ Microbiol] 2020 Apr; Vol. 22 (4), pp. 1280-1293. Date of Electronic Publication: 2020 Feb 07.
  • Publication Type:
    Journal Article; Research Support, Non-U.S. Gov't
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Blackwell Science Country of Publication: England NLM ID: 100883692 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1462-2920 (Electronic) Linking ISSN: 14622912 NLM ISO Abbreviation: Environ Microbiol Subsets: MEDLINE
    • Publication Information:
      Original Publication: Oxford : Blackwell Science, 1999-
    • Subject Terms:
    • Abstract:
      Streets are constantly crossed by billions of vehicles and pedestrians. Their gutters, which convey stormwater and contribute to waste management, and are important for human health and well-being, probably play a number of ecological roles. Street surfaces may also represent an important part of city surface areas. To better characterize the ecology of this yet poorly explored compartment, we used filtration and DNA metabarcoding to address microbial community composition and assembly across the city of Paris, France. Diverse bacterial and eukaryotic taxonomic groups were identified, including members involved in key biogeochemical processes, along with a number of parasites and putative pathogens of human, animals and plants. We showed that the beta diversity patterns between bacterial and eukaryotic communities were correlated, suggesting interdomain associations. Beta diversity analyses revealed the significance of biotic factors (cohesion metrics) in shaping gutter microbial community assembly and, to a lesser extent, the contribution of abiotic factors (pH and conductivity). Co-occurrences analysis confirmed contrasting non-random patterns both within and between domains of life, specifically when comparing diatoms and fungi. Our results highlight microbial coexistence patterns in streets and reinforce the need to further explore biodiversity in urban ground transportation infrastructures.
      (© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.)
    • References:
      Adamiak, J., Otlewska, A., Tafer, H., Lopandic, K., Gutarowska, B., Sterflinger, K., and Pinar, G. (2018) First evaluation of the microbiome of built cultural heritage by using the Ion Torrent next generation sequencing platform. Int Biodeter Biodegr 131: 11-18.
      Afshinnekoo, E., Meydan, C., Chowdhury, S., Jaroudi, D., Boyer, C., Bernstein, N., et al. (2015) Geospatial resolution of human and bacterial diversity with city-scale metagenomics. Cell Syst 1: 72-87.
      Allen, J.L., Leflaive, J., Bringuier, C., Ten-Hage, L., Chauvet, E., Cornut, J., and Danger, M. (2017) Allelopathic inhibition of primary producer growth and photosynthesis by aquatic fungi. Fungal Ecol 29: 133-138.
      Amato, P., Joly, M., Besaury, L., Oudart, A., Taib, N., Mone, A.I., et al. (2017) Active microorganisms thrive among extremely diverse communities in cloud water. PLOS One 12: e.0182869.
      Amin, S.A., Parker, M.S., and Armbrust, E.V. (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76: 667-684.
      Baral, D., Speicher, A., Dvorak, B., Admiraal, D., and Li, X. (2018) Quantifying the relative contributions of environmental sources to the microbial community in an urban stream under dry and wet weather conditions. Appl Environ Microbiol 84(15): e00896-18.
      Battin, T.J., Besemer, K., Bengtsson, M.M., Romani, A.M., and Packmann, A.I. (2016) The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol 14: 251-263.
      Bertelli, C., Courtois, S., Rosikiewicz, M., Piriou, P., Aeby, S., Robert, S., et al. (2018) Reduced chlorine in drinking water distribution systems impacts bacterial biodiversity in biofilms. Front Microbiol 9: 2520.
      Besemer, K. (2015) Biodiversity, community structure and function of biofilms in stream ecosystems. Res Microbiol 166: 774-781.
      Birtles, R.J., Rowbotham, T.J., Michel, R., Pitcher, D.G., Lascola, B., Alexiou-Daniel, S., and Raoult, D. (2000) 'Candidatus Odyssella thessalonicensis' gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int J Syst Evol Microbiol 50: 63-72.
      Bruno, A., Sandionigi, A., Bernasconi, M., Panio, A., Labra, M., and Casiraghi, M. (2018) Changes in the drinking water microbiome: effects of water treatments along the flow of two drinking water treatment plants in a urbanized area, Milan (Italy). Front Microbiol 9: 2557.
      Buchan, A., LeCleir, G.R., Gulvik, C.A., and Gonzalez, J.M. (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12: 686-698.
      Calderon, O., Porter-Morgan, H., Jacob, J., and Elkins, W. (2017) Bacterial diversity impacts as a result of combined sewer overflow in a polluted waterway. Global J Environ Sci Manage 3: 437-446.
      Cavalier-Smith, T., and Chao, E.E. (2003) Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154: 341-358.
      Cayford, B.I., Jiang, G.M., Keller, J., Tyson, G., and Bond, P.L. (2017) Comparison of microbial communities across sections of a corroding sewer pipe and the effects of wastewater flooding. Biofouling 33: 780-792.
      Chimienti, G., Piredda, R., Pepe, G., van der Werf, I.D., Sabbatini, L., Crecchio, C., et al. (2016) Profile of microbial communities on carbonate stones of the medieval church of San Leonardo di Siponto (Italy) by Illumina-based deep sequencing. Appl Microbiol Biotechnol 100: 8537-8548.
      Cowle, M.W., Babatunde, A.O., and Bockelmann-Evans, B.N. (2017) The frictional resistance induced by bacterial based biofouling in drainage pipelines. J Hydraul Res 55: 269-283.
      Doilom, M., Liu, J.K., Jaklitsch, W.M., Ariyawansa, H., Wijayawardene, N.N., Chukeatirote, E., et al. (2013) An outline of the family Cucurbitariaceae. Sydowia 65: 167-192.
      Domingo, J.W.S., Revetta, R.P., Iker, B., Gomez-Alvarez, V., Garcia, J., Sullivan, J., and Weast, J. (2011) Molecular survey of concrete sewer biofilm microbial communities. Biofouling 27: 993-1001.
      Dong, S.F., and Yao, M.S. (2010) Exposure assessment in Beijing, China: biological agents, ultrafine particles, and lead. Environ Monit Assess 170: 331-343.
      Douterelo, I., Fish, K.E., and Boxall, J.B. (2018) Succession of bacterial and fungal communities within biofilms of a chlorinated drinking water distribution system. Water Res 141: 74-85.
      Douterelo, I., Sharpe, R.L., Husband, S., Fish, K.E., and Boxall, J.B. (2019) Understanding microbial ecology to improve management of drinking water distribution systems. Wiley Interdiscip Rev-Water 6: e1325.
      Drury, B., Rosi-Marshall, E., and Kelly, J.J. (2013) Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Appl Environ Microbiol 79: 1897-1905.
      Dybwad, M., Granum, P.E., Bruheim, P., and Blatny, J.M. (2012) Characterization of airborne bacteria at an underground subway station. Appl Environ Microbiol 78: 1917-1929.
      Dybwad, M., Skogan, G., and Blatny, J.M. (2014) Temporal variability of the bioaerosol background at a subway station: concentration level, size distribution, and diversity of airborne bacteria. Appl Environ Microbiol 80: 257-270.
      Dyda, M., Decewicz, P., Romaniuk, K., Wojcieszak, M., Sklodowska, A., Dziewit, L., et al. (2018) Application of metagenomic methods for selection of an optimal growth medium for bacterial diversity analysis of microbiocenoses on historical stone surfaces. Int Biodeter Biodegr 131: 2-10.
      Fan, H.Q., Li, X.Y., Deng, J.H., Da, G., Gehin, E., and Yao, M.S. (2017) Time-dependent size-resolved bacterial and fungal aerosols in Beijing subway. Aerosol Air Qual Res 17: 799-809.
      Flemming, H.C., and Wuertz, S. (2019) Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17: 247-260.
      Fresia, P., Antelo, V., Salazar, C., Gimenez, M., D'Alessandro, B., Afshinnekoo, E., et al. (2019) Urban metagenomics uncover antibiotic resistance reservoirs in coastal beach and sewage waters. Microbiome 7: 35.
      Garvette, A., Nezan, E., Badis, Y., Bilien, G., Arce, P., Bresnan, E., et al. (2018) Novel widespread marine Oomycetes parasitising diatoms, including the toxic genus Pseudo-nitzschia: genetic, morphological, and ecological characterisation. Front Microbiol 9: 2918.
      Gaylarde, C., Baptista-Neto, J.A., Ogawa, A., Kowalski, M., Celikkol-Aydin, S., and Beech, I. (2017) Epilithic and endolithic microorganisms and deterioration on stone church facades subject to urban pollution in a sub-tropical climate. Biofouling 33: 113-127.
      Gomez-Alvarez, V., Humrighouse, B.W., Revetta, R.P., and Domingo, J.W.S. (2015) Bacterial composition in a metropolitan drinking water distribution system utilizing different source waters. J Water Health 13: 140-151.
      Goslee, S.C., and Urban, D.L. (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22: 1-19.
      Griffith, D.M., Veech, J.A., and Marsh, C.J. (2016) Cooccur: probabilistic species co-occurrence analysis in R. J Stat Software 69: 1-17.
      Grossart, H.P., Wurzbacher, C., James, T.Y., and Kagami, M. (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecol 19: 28-38.
      Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L., et al. (2013) The Protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41: D597-D604.
      Hanson, C.A., Fuhrman, J.A., Horner-Devine, M.C., and Martiny, J.B. (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10: 497-506.
      Herlemann, D.P., Labrenz, M., Jurgens, K., Bertilsson, S., Waniek, J.J., and Andersson, A.F. (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5: 1571-1579.
      Herren, C.M., and McMahon, K.D. (2017) Cohesion: a method for quantifying the connectivity of microbial communities. ISME J 11: 2426-2438.
      Herren, C.M., and McMahon, K.D. (2018) Keystone taxa predict compositional change in microbial communities. Environ Microbiol 20: 2207-2217.
      Hervé, V., Leroy, B., Da Silva Pires, A., and Lopez, P.J. (2018) Aquatic urban ecology at the scale of a capital: community structure and interactions in street gutters. ISME J 12: 253-266.
      Hsu, T., Joice, R., Vallarino, J., Abu-Ali, G., Hartmann, E.M., Shafquat, A., et al. (2016) Urban transit system microbial communities differ by surface type and interaction with humans and the environment. Msystems 1(3): e00018-16.
      Jaklitsch, W.M., Checa, J., Blanco, M.N., Olariaga, I., Tello, S., and Voglmayr, H. (2018) A preliminary account of the Cucurbitariaceae. Stud Mycol 90: 71-118.
      Janke, B.D., Finlay, J.C., and Hobbie, S.E. (2017) Trees and streets as drivers of urban stormwater nutrient pollution. Environ Sci Technol 51: 9569-9579.
      Jiang, G.M., Zhou, M., Chiu, T.H., Sun, X.Y., Keller, J., and Bond, P.L. (2016) Wastewater-enhanced microbial corrosion of concrete sewers. Environ Sci Technol 50: 8084-8092.
      Johnsen, A.R., de Lipthay, J.R., Reichenberg, F., Sorensen, S.J., Andersen, O., Christensen, P., et al. (2006) Biodegradation, bioaccessibility, and genotoxicity of diffuse polycyclic aromatic hydrocarbon (PAH) pollution at a motorway site. Environ Sci Technol 40: 3293-3298.
      Johnsen, A.R., Styrishave, B., and Aamand, J. (2014) Quantification of small-scale variation in the size and composition of phenanthrene-degrader populations and PAH contaminants in traffic-impacted topsoil. FEMS Microbiol Ecol 88: 84-93.
      Kachour, L., Gacemi-Kirane, D., Loucif, L., and Alayat, H. (2016) First survey of aquatic microbial Fungi-like Pythiaceae predominantly colonizing the south-Mediterranean freshwater wetlands. Res J Pharm Biol Chem Sci 7: 3067-3078.
      Kembel, S.W., Jones, E., Kline, J., Northcutt, D., Stenson, J., Womack, A.M., et al. (2012) Architectural design influences the diversity and structure of the built environment microbiome. ISME J 6: 1469-1479.
      Khreis, H., Warsow, K.M., Verlinghieri, E., Guzman, A., Pellecuer, L., Ferreira, A., et al. (2016) The health impacts of traffic-related exposures in urban areas: understanding real effects, underlying driving forces and co-producing future directions. J Transp Health 3: 249-267.
      Kindaichi, T., Yamaoka, S., Uehara, R., Ozaki, N., Ohashi, A., Albertsen, M., et al. (2016) Phylogenetic diversity and ecophysiology of Candidate phylum Saccharibacteria in activated sludge. FEMS Microbiol Ecol 92: fiw078.
      Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K., and Schloss, P.D. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79: 5112-5120.
      Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
      Kuhn, S.F., and Hofmann, M. (1999) Infection of Coscinodiscus granii by the parasitoid nanoflagellate Pirsonia diadema: III. Effects of turbulence on the incidence of infection. J Plankton Research 21: 2323-2340.
      Leonard, G., Labarre, A., Milner, D.S., Monier, A., Soanes, D., Wideman, J.G., et al. (2018) Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides. Open Biol 8: 170184.
      Leung, M.H., Wilkins, D., Li, E.K., Kong, F.K., and Lee, P.K. (2014) Indoor-air microbiome in an urban subway network: diversity and dynamics. Appl Environ Microbiol 80: 6760-6770.
      Li, H., Liu, D.F., Lian, B., Sheng, Y., and Dong, H.L. (2012) Microbial diversity and community structure on corroding concretes. Geomicrobiol J 29: 450-458.
      Li, X., Kappler, U., Jiang, G.M., and Bond, P.L. (2017) The ecology of acidophilic microorganisms in the corroding concrete sewer environment. Front Microbiol 8: 683.
      Marques, E.L.S., Silva, G.S., Dias, J.C.T., Gross, E., Costa, M.S., and Rezende, R.P. (2019) Cave drip water-related samples as a natural environment for aromatic hydrocarbon-degrading bacteria. Microorganisms 7: 33.
      McLellan, S.L., and Roguet, A. (2019) The unexpected habitat in sewer pipes for the propagation of microbial communities and their imprint on urban waters. Curr Opin Biotechnol 57: 34-41.
      Meng, S.W., Torto-Alalibo, T., Chibucos, M.C., Tyler, B.M., and Dean, R.A. (2009) Common processes in pathogenesis by fungal and oomycete plant pathogens, described with gene ontology terms. BMC Microbiol 9: S7.
      Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., et al. (2015) vegan: community ecology package. R package version 2.3-2. In: http://CRAN.R-project.org/package=vegan.
      Patel, K.V., Bailey, C.L., Harding, A.H., Biggin, M., and Crook, B. (2018) Background levels of micro-organisms in the busy urban environment of transport hubs. J Appl Microbiol 125: 1541-1551.
      Pedron, R., Esposito, A., Bianconi, I., Pasolli, E., Tett, A., Asnicar, F., et al. (2019) Genomic and metagenomic insights into the microbial community of a thermal spring. Microbiome 7: 8.
      Perlman, S.J., Hunter, M.S., and Zchori-Fein, E. (2006) The emerging diversity of rickettsia. Proc Biol Sci 273: 2097-2106.
      Perrin, Y., Bouchon, D., Delafont, V., Moulin, L., and Hechard, Y. (2019) Microbiome of drinking water: a full-scale spatio-temporal study to monitor water quality in the Paris distribution system. Water Res 149: 375-385.
      Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
      Ragon, M., Restoux, G., Moreira, D., Moller, A.P., and Lopez-Garcia, P. (2011) Sunlight-exposed biofilm microbial communities are naturally resistant to chernobyl ionizing-radiation levels. PLoS One 6: e21764.
      Reblova, M., Hubka, V., Thureborn, O., Lundberg, J., Sallstedt, T., Wedin, M., and Ivarsson, M. (2016) From the tunnels into the treetops: new lineages of black yeasts from biofilm in the Stockholm metro system and their relatives among ant-associated fungi in the Chaetothyriales. PLoS One 11: e0163396.
      Richard, C., Mitbavkar, S., and Landoulsi, J. (2017) Diagnosis of the diatom community upon biofilm development on stainless steels in natural freshwater. Scanning 2017: 5052646.
      Rognes, T., Flouri, T., Nichols, B., Quince, C., and Mahe, F. (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4: e2584.
      Sanchez-Gonzalez, M., Alvarez-Uribe, H., Rivera-Solis, R., Gonzalez-Burgos, A., Escalante-Rendiz, D., and Rojas-Herrera, R. (2019) Analysis of a phenol-adapted microbial community: degradation capacity, taxonomy and metabolic description. J Appl Microbiol 126: 771-779.
      Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
      Scholz, B., Guillou, L., Marano, A.V., Neuhauser, S., Sullivan, B.K., Karsten, U., et al. (2016) Zoosporic parasites infecting marine diatoms - a black box that needs to be opened. Fungal Ecol 19: 59-76.
      Shamarina, D., Stoyantcheva, I., Mason, C.E., Bibby, K., and Elhaik, E. (2017) Communicating the promise, risks, and ethics of large-scale, open space microbiome and metagenome research. Microbiome 5: 132.
      Shi, T., Fredrickson, J.K., and Balkwill, D.L. (2001) Biodegradation of polycyclic aromatic hydrocarbons by Sphingomonas strains isolated from the terrestrial subsurface. J Ind Microbiol Biotechnol 26: 283-289.
      Siddaramappa, S., Viswanathan, V., Thiyagarajan, S., and Narjala, A. (2018) Genomewide characterisation of the genetic diversity of carotenogenesis in bacteria of the order Sphingomonadales. Microbial Genomics 4: 172.
      Sison-Mangus, M.P., Jiang, S., Tran, K.N., and Kudela, R.M. (2014) Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. ISME J 8: 63-76.
      Tesei, D., Tafer, H., Poyntner, C., Pinar, G., Lopandic, K., and Sterflinger, K. (2017) Draft genome sequences of the black rock fungus Knufia petricola and its spontaneous nonmelanized mutant. Genome Announc 5: e01242-17.
      van Tol, H.M., Amin, S.A., and Armbrust, E.V. (2017) Ubiquitous marine bacterium inhibits diatom cell division. ISME J 11: 31-42.
      Veech, J.A. (2013) A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr 22: 252-260.
      Voisin, J., Cournoyer, B., Vienney, A., and Mermillod-Blondin, F. (2018) Aquifer recharge with stormwater runoff in urban areas: influence of vadose zone thickness on nutrient and bacterial transfers from the surface of infiltration basins to groundwater. Sci Total Environ 637: 1496-1507.
      Wang, H.T., Cheng, M.Y., Dsouza, M., Weisenhorn, P., Zheng, T.L., and Gilbert, J.A. (2018) Soil bacterial diversity is associated with human population density in urban greenspaces. Environ Sci Technol 52: 5115-5124.
      Wang, Y., Naumann, U., Wright, S.T., and Warton, D.I. (2012) Mvabund- an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3: 471-474.
      Warton, D.I., Wright, S.T., and Wang, Y. (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3: 89-101.
      Weiss, S., Xu, Z.Z., Peddada, S., Amir, A., Bittinger, K., Gonzalez, A., et al. (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5: 27.
      Westcott, S.L., and Schloss, P.D. (2017) OptiClust, an improved method for assigning amplicon-based sequence data to operational taxonomic units. Msphere 2(2): e00073-17.
      Zhang, J., Wei, Z., Jia, H.F., and Huang, X. (2017) Factors influencing water quality indices in a typical urban river originated with reclaimed water. Front Environ Sci Eng 11: 8.
      Zhang, S.H., Pang, S., Wang, P.F., Wang, C., Han, N.N., Liu, B., et al. (2016) Antibiotic concentration and antibiotic-resistant bacteria in two shallow urban lakes after stormwater event. Environ Sci Pollut Res 23: 9984-9992.
    • Publication Date:
      Date Created: 20200131 Date Completed: 20201119 Latest Revision: 20201119
    • Publication Date:
      20221213
    • Accession Number:
      10.1111/1462-2920.14933
    • Accession Number:
      31997567