Aerobiology of the built environment: Synergy between Legionella and fungi


      • In built environments Legionella can establish a synergistic relationship with fungi.
      • Fungi can help in the dissemination of Legionella in indoor environments.
      • Legionella cells aerosolized with fungi are less prone to ultraviolet disinfection.


      The modern built environment (BE) design creates unique ecological niches ideal for the survival and mutual interaction of microbial communities. This investigation focused on the synergistic relations between Legionella and the fungal species commonly found in BEs and the impact of these synergistic relationships on the survival and transmission of Legionella.


      A field study was conducted to identify the types and concentrations of fungi in BEs. The fungal isolates purified from BEs were cocultured with Legionella to study their synergistic association. Cocultured Legionella cells were aerosolized in an air-tight chamber to evaluate the efficacy of ultraviolet (UV) to inactivate these cells.


      Aspergillus, Alternaria, and Cladosporium were the most common fungi detected in samples that tested positive for Legionella. After coculturing, Legionella cells were detected inside fungal hyphae. The microscopic observations of Legionella internalization in fungal hyphae were confirmed by molecular analyses. UV disinfection of the aerosolized Legionella cells that were cocultured with fungi indicated that fungal spores and propagules act as a shield against UV radiation. The shield effect of fungal spores on Legionella cells was quantified at >2.5 log10.


      This study provides the first evidence, to our knowledge, of Legionella cell presence inside fungi detected in an indoor environment. This symbiotic relationship with fungi results in longer survival of Legionella under ambient conditions and provides protection against UV rays.

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        • Chao H.J.
        • Schwartz J.
        • Milton D.K.
        • Burge H.A.
        The work environment and workers health in four large office buildings.
        Environ Health Perspect. 2003; 111: 1242-1248
        • Molhave L.
        Sick building syndrome.
        in: Nriagu J.O. Encyclopedia of environmental health. Elsevier Science, Philadelphia (PA)2011: 61-67
        • Ebbehøj N.E.
        • Hansen M.O.
        • Sigsgaard T.
        • Larsen L.
        Building-related symptoms and molds: a two-step intervention study.
        Indoor Air. 2002; 12: 273-277
        • Zeliger H.I.
        Toxic effects of chemical mixtures.
        Arch Environ Health. 2003; 58: 23-29
        • Nevalainen A.
        • Seuri M.
        Of microbes and men.
        Indoor Air. 2005; 15: 58-64
        • Khan A.A.H.
        • Karuppayil S.M.
        Potential natural disinfectants for indoor environments.
        Int J Clin Aromather. 2010; 7: 1-5
        • Samet J.M.
        • Spengler J.D.
        Indoor environments and health: moving into the 21st century.
        Am J Pub Health. 2003; 93: 1489-1493
        • Khan A.A.H.
        • Karuppayil S.M.
        Fungal pollution of indoor environments and its management.
        Saudi J Biol Sci. 2012; 19: 405-426
        • Portnoy J.M.
        Evaluation of indoor mold exposure is what allergists do best.
        Ann Allergy Asthma Immunol. 2003; 90: 175
        • Brunkard J.M.
        • Ailes E.
        • Roberts V.A.
        • Hill V.
        • Hilborn E.D.
        • Craun G.F.
        • et al.
        Surveillance for waterborne disease outbreaks associated with drinking water—United States, 2007-2008.
        MMWR Morb Mortal Wkly Rep. 2011; 60: 38-68
        • Nakayama K.
        • Morimoto K.
        Relationship between, lifestyle, mold and sick building syndromes in newly built dwellings in Japan.
        Int J Immunopathol Pharmacol. 2007; 20: 35-43
        • US Environmental Protection Agency, Office of Water
        Legionella human health criteria document.
        US Environmental Protection Agency, Office of Water, Washington (DC)1999
        • Beer K.D.
        • Gargano J.W.
        • Roberts V.A.
        • Hill V.
        • Garrison L.
        • Kutty P.
        • et al.
        Surveillance for waterborne disease outbreaks associated with drinking water—United States, 2011-2012.
        MMWR Morb Mortal Wkly Rep. 2015; 64: 842-848
        • Fischer P.H.
        • Kriz B.
        • Martuzzi M.
        • Wojtyniak B.
        • Lebret E.
        • Van Reeuwijk H.
        • et al.
        Risk factors indoors and prevalences of childhood respiratory health in four countries in western and central Europe.
        Indoor Air. 1988; 8: 244-254
        • Garrett M.H.
        • Rayment P.R.
        • Hooper M.A.
        • Abramson M.J.
        Indoor airborne fungal spores, house dampness and associations with environmental factors and respiratory health in children.
        Clin Exp Allergy. 1988; 28: 459-467
        • Kozak P.P.
        • Gallup J.
        • Cummins L.H.
        • Gillman S.A.
        Factors of importance in determining the prevalence of indoor molds.
        Ann Allergy. 1980; 43: 88-94
        • Rylander R.
        • Megevand Y.
        Environmental risk factors for respiratory infections.
        Arch Environ Health. 2000; 55: 300-303
        • Reijula K.
        Moisture-problem buildings with molds causing work-related diseases.
        Adv Appl Microbiol. 2004; 55: 175-189
        • Hatfield M.L.
        • Hartz K.E.H.
        Secondary organic aerosol from biogenic volatile organic compounds mixtures.
        Atmos Environ. 2011; 45: 2211-2219
        • Pieckova E.
        • Jesenska Z.
        Microscopic fungi in dwellings and their health implications in humans.
        Ann Agric Environ Med. 1999; 6: 1-11
        • Anaissie E.J.
        • Penzak S.R.
        • Dignani M.C.
        The hospital water supply as a source of nosocomial infections: a plea for action.
        Arch Intern Med. 2002; 162: 1483-1492
        • Casini B.
        • Valentini P.
        • Baggiani A.
        • Torracca F.
        • Frateschi S.
        • Nelli L.C.
        • et al.
        Molecular epidemiology of Legionella pneumophila serogroup 1 isolates following long-term chlorine dioxide treatment in a university hospital water system.
        J Hosp Infect. 2008; 69: 141-147
        • Szewzyk U.
        • Szewzyk R.
        • Manz W.
        • Schleifer K.H.
        Microbiological safety of drinking water.
        Annu Rev Microbiol. 2000; 54: 81-127
        • Steele T.W.
        • Lanser J.
        • Sangster N.
        Isolation of Legionella longbeachae serogroup 1 from potting mixes.
        Appl Environ Microbiol. 1990; 56: 49-53
        • Stryjakowska-Sekulska M.
        • Piotraszewska-Pająk A.
        • Szyszka A.
        • Nowicki M.
        • Filipiak M.
        Microbiological quality of indoor air in university rooms.
        Pol J Environ Stud. 2007; 16: 624-632
        • O'Meara T.
        • Tovey E.
        Monitoring personal allergen exposure.
        Clin Rev Allergy Immunol. 2000; 18: 341-395
        • Reponen T.
        • Singh U.
        • Schaffer C.
        • Vesper S.
        • Johansson E.
        • Adhikari A.
        • et al.
        Visually observed mold and moldy odor versus quantitatively measured microbial exposure in homes.
        Sci Total Environ. 2010; 408: 5565-5574
        • Zafar S.
        • Aqil F.
        • Ahmad I.
        Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agriculture soil.
        Bioresour Technol. 2007; 98: 2557-2561
        • US Department of Health and Human Services, Centers for Disease Control and Prevention
        Procedures for the recovery of Legionella from the environment.
        2005 (Available from:) (Accessed April 17, 2016)
        • Wullings B.A.
        • Bakker G.
        • van der Kooij D.
        Concentration and diversity of uncultured Legionella spp. in two unchlorinated drinking water supplies with different concentrations of natural organic matter.
        Appl Environ Microbiol. 2011; 77: 634-641
        • King B.
        • Kesavan J.
        • Sagripanti J.-L.
        Germicidal UV sensitivity of bacteria in aerosols and on contaminated surfaces.
        Aerosol Sci Technol. 2011; 45: 1-9
        • Hargreaves M.
        • Parappukkaran S.
        • Morawska L.
        • Hitchins J.
        • Congrong H.
        • Gilbert D.
        A pilot investigation into associations between indoor airborne fungal and nonbiological particle concentrations in residential houses in Brisbane.
        Sci Total Environ. 2003; 312: 89-101
        • Srikanth P.
        • Sudharsanam S.
        • Steinberg R.
        Bioaerosols in indoor environment: composition, health effects and analysis.
        Indian J Med Microbiol. 2008; 26: 302-312
        • Tsai F.C.
        • Macher J.M.
        Concentrations of airborne culturable bacteria in 100 large US office buildings from the BASE study.
        Indoor Air. 2005; 15: 71-81
        • Ojima M.
        • Toshima Y.
        • Koya E.
        • Ara K.
        • Tokuda H.
        Hygiene measures considering actual distributions of microorganisms in Japanese households.
        J Appl Microbiol. 2002; 93: 800-809
        • Hamada N.
        • Abe N.
        Growth characteristics of fungal species from bathroom.
        Biocontrol Sci. 2010; 15: 111-115
        • Montagna M.T.
        • De Giglio O.
        • Napoli C.
        • Cannova L.
        • Cristina M.L.
        • Deriu M.G.
        • et al.
        Legionella spp. contamination in indoor air: preliminary results of an Italian multicenter study.
        Epidemiol Prev. 2014; 38: 62-65
        • Fonseca M.V.
        • Swanson M.S.
        Nutrient salvaging and metabolism by the intracellular pathogen Legionella pneumophila.
        Front Cell Infect Microbiol. 2014; 4: 12
        • Aurass P.
        • Schlegel M.
        • Metwally O.
        • Harding C.R.
        • Schroeder G.N.
        • Frankel G.
        • et al.
        The Legionella pneumophila Dot/Icm-secreted effector PlcC/CegC1 together with PlcA and PlcB promotes virulence and belongs to a novel zinc metallophospholipase C family present in bacteria and fungi.
        J Biol Chem. 2013; 288: 11080-11092
        • Alfano J.R.
        • Collmer A.
        Type III secretion system effector proteins: double agents in bacterial disease and plant defense.
        Annu Rev Phytopathol. 2004; 42: 385-414
        • Burstein D.
        • Zusman T.
        • Degtyar E.
        • Viner R.
        • Segal G.
        • Pupko T.
        Genome-scale identification of Legionella pneumophila effectors using a machine learning approach.
        PLoS Pathog. 2009; 5: e1000508
        • Huang L.
        • Boyd D.
        • Amyot W.M.
        • Hempstead A.D.
        • Luo Z.Q.
        • O'Connor T.J.
        • et al.
        The E block motif is associated with Legionella pneumophila translocated substrates.
        Cell Microbiol. 2010; 13: 227-245
        • D'Auria G.
        • Jiménez-Hernández N.
        • Peris-Bondia F.
        • Moya A.
        • Latorre A.
        Legionella pneumophila pangenome reveals strain-specific virulence factors.
        BMC Genomics. 2010; 11: 181
        • Engel J.
        • Balachandran P.
        Role of Pseudomonas aeruginosa type III effectors in disease.
        Curr Opin Microbiol. 2009; 12: 61-66
        • Newton H.J.
        • Ang D.K.Y.
        • van Driel I.R.
        • Hartland E.L.
        Molecular pathogenesis of infections caused by Legionella pneumophila.
        Clin Microbiol Rev. 2010; 23: 274-298
        • de Ana S.G.
        • Torres-Rodriguez J.M.
        • Ramirez E.A.
        • Garcia S.M.
        • Belmonte-Soler J.
        Seasonal distribution of Alternaria, Aspergillus, Cladosporium and Penicillium species isolated in homes of fungal allergic patients.
        J Investig Allergol Clin Immunol. 2006; 16: 357-363
        • Haleem Khan A.A.
        • Mohan Karuppayil S.
        Fungal pollution of indoor environments and its management.
        Saudi J Biol Sci. 2012; 19: 405-426
        • Ren P.
        • Jankun T.M.
        • Belanger K.
        • Bracken M.B.
        • Leaderer B.P.
        The relation between fungal propagules in indoor air and home characteristics.
        Allergy. 2001; 56: 419-424
        • Khandpur R.S.
        Handbook of biomedical instrumentation.
        Tata McGraw-Hill Education, New Delhi, India2003
        • Barker K.A.
        • Whitney E.A.
        • Blake S.
        • Berkelman R.L.
        A review of guidelines for the primary prevention of legionellosis in long-term care facilities.
        J Am Med Dir Assoc. 2015; 16: 832-836
        • Coohill T.P.
        Virus cell interactions as probes for vacuum-ultraviolet radiation damage and repair.
        Photochem Photobiol. 1986; 44: 359-363
        • Coohill T.P.
        • Sagripanti J.L.
        Bacterial inactivation by solar ultraviolet radiation compared with sensitivity to 254 nm radiation.
        Photochem Photobiol. 2009; 85: 1043-1052