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. 2023 Dec 27;2(1):34–41. doi: 10.1021/envhealth.3c00145

ITS and 16S rRNA Gene Revealed Multitudinous Microbial Contaminations of Residential Air Conditioning Filters in Megacity Shanghai, China

Xueyun Geng †, Changliang Nie †,*, Lina Wang †, Ling Li †, Dan Li †, Atsushi Nishino ‡, Jianmin Chen †,§,∥,*
PMCID: PMC11503804  PMID: 39473487

Abstract

graphic file with name eh3c00145_0005.jpg

Air conditioning is a crucial participant in indoor air circulation and harmful microorganism transmission. To elucidate microbial contamination in air conditioning systems, bacteria, fungi, and pollens in residential air conditioning (AC) filters in Shanghai were revealed. The concentrations of fungal ITS (1,972,037 ± 5,025,505 copies/cm2) in most filter samples were considerably higher than the 16S rRNA gene (21,587 ± 21,461 copies/cm2). The multitudinous bacteria determined a higher richness, whereas the trend was not in line with fungi, owing to Aspergillus flourishing, with an average of 43.75%. Numerous bacteria that may often be prevalent in human skin, mucous membranes, and intestines, such as Enhydrobacter, Micrococcus, Staphylococcus, Streptococcus, and Haemophilus, were also discovered in AC filters. The pollens were affiliated with Streptophyta at phylum, and Humulus was the most abundant genus (mean value 67.84%), raising the possibility of allergic responses. This study provides a better understanding of the microbial characteristics of AC filters, enables more rational approaches for microbe contaminant control, and ultimately improves human health in megacities.

Keywords: air conditioning system, indoor air, building microbiome, DNA sequencing, pathogens

1. Introduction

Indoor air contains not only chemical constituents but also microbiomes.1 This sparked topical alarm over the importance of indoor microbiomes, especially in indoor environments, since most people spend more than 90% of their lives inside buildings.2 The microorganism-associated contamination could account for approximately 21% of indoor air issues, including bacteria, viruses, fungi, small protozoa, and microalgae, which can cause discomfort and health problems.3,4 The heating, ventilation, and air conditioning (HVAC) system, one of the spots easily invaded by microorganisms, must be considered because of the increasingly expanding use of air conditioning.1,3

Researchers have estimated the microbe distribution in HVAC systems.4−9 For instance, prior studies have found that microbial ecologies on air conditioning cooling coils are influenced by climate and operating parameters,8 and the bacterial and fungal concentrations of this part in the USA were 1.2 × 107 cells/m2 and 7.6 × 105 spore equivalents (SE)/m2, respectively.10 The Staphylococcus and Micrococcus, two antibiotic-resistant bacteria, were abundant in the HVAC dust samples from kindergartens in Hong Kong.11 The fungal spores concentration was detected as high as 104 CFU/m3 near the outlet of the HVAC system, which significantly suppressed China’s national indoor hygiene standard limit (2,500 CFU/m3).3 These findings all pointed out that HVAC was a non-negligible source of indoor microbial contamination. Besides that, airborne pollen is also a critical component of bioaerosol which causes pneumonia, chronic obstructive pulmonary, cardiovascular, and allergic respiratory diseases.12 The morbidity rate of pollen allergy is estimated at 40% in Europe,13 while the value rose to 47.8% in China.14 These active airborne particles could be captured by HVAC filters.4,15 The gathered microorganisms on filter surfaces can use nutrients from dust to grow at appropriate temperatures and humidity. These microbiotas would be aerosolized when occupants switch on the air conditioner, posing potential threats to human health.16 Unfortunately, the microbiota distribution in HVAC filters has not yet been adequately addressed, to the best of our knowledge. There are still gaps aimed at microbial contaminants in residential HVAC filters that need to be filled.

A typical megacity of the Yangtze River region, Shanghai, China, with a crucial role in the economy and a substantial need for cooling and heating, was selected as the sampling site.17 The main objective of this study was to quantify the concentrations of bacteria and fungi on the surfaces of the AC filters and explore the bacteria, fungi, and pollen community by next-generation high-throughput sequencing technologies. The insights gained in the present work can offer a comprehensive understanding of the microbiome distribution of AC filters, providing practical approaches to assess indoor air quality in several houses without discomfort to the residents by the traditional sampling method.

2. Materials and Methods

2.1. Sample Collection and Pretreatment

To investigate microbial contaminations in domestic air-conditioning systems, seven AC filters were randomly collected from four households (namely, F1–F4) in different locations in Shanghai during October 21–28, 2021 (Table S2). The sampling procedures are described in detail in the Supporting Information (Text S1). All filters were cut into several pieces, generally 100 cm2 each (10 cm × 10 cm), as shown in Figure 1a, followed by extraction, and enrichment for downstream bioinformatics analysis.

Figure 1.

Figure 1

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(a) Overall experimental schematic in this study. Black ink represents workflows; red shows main lab procedures. (b) Concentrations (log10 copies/cm2) of bacteria using qPCR tests and bacterial Chao index for six filters from each family. Relative abundances of (c) bacterial phylum and (d) bacterial genera of samples in Shanghai.

2.2. DNA Extraction and MiSeq Sequencing

Genomic DNA was extracted using the E.Z.N.A. soil DNA Kit (Omega Bio-tek, Norcross, GA, U.S.). The bacteria 16S rRNA gene V3–V4 hypervariable region, fungal ITS rDNA genes and the plant-specific internal transcribes spacer 2 (ITS2) region were amplified using the 338F/806R,18 ITS1/ITS2,19 and ITS-p3/ITS-u420 as primer pair, respectively (Text S1 and Table S1). Sequencing was performed on an Illumina MiSeq PE300 instrument (Illumina, San Diego, CA, USA) with MiSeq reagent kit V3 (Illumina) according to the standard protocols. Quantitative PCR (qPCR) was performed to quantify the fungal or bacterial gene copies per square centimeter of AC filters. Additional experimental details are provided in the Supporting Information and described in detail elsewhere.

2.3. Data Analysis

Operational taxonomic units (OTUs) were clustered with 97% similarity cutoff using UPARSE (version 7.1 http://drive5.com/uparse/), and chimeric sequences were identified and removed. The OTUs were further assigned into different taxonomic categories against the SILVA database,21 Unite ITS database,22 and ITS2 database23 for bacteria, fungi, and pollen, respectively. Alpha diversity, including observed species, Ace, Chao1, Shannon, Simpson, and Good’s coverage, were calculated to investigate the differences and variations in bacterial, fungal, and pollen diversity and richness in AC filters by QIIME (V1.9.1). The bacterial functions and phenotypes including oxygen utilization (aerobic, anaerobic, or facultatively anaerobic), Gram classification, biofilm-forming ability, mobile element content, potential pathogenicity, and stress tolerance, were predicted by the BugBase (https://bugbase.cs.umn.edu/) at the organism level.24

3. Results and Discussion

3.1. Bacterial Concentration, Community Structures, and Functions

As shown in Figure 1b, the bacterial concentration obviously varied, ranging from 103 to 104 copies/cm2. It is speculated that the variation in the absolute concentration of bacteria or fungi is probably subject to the frequency of AC use or filter cleaning. The bacterial/fungal counts can be estimated by 16S rRNA genes/ITS gene using 4.6/200 as an average DNA copy number,25 indicating high cell numbers on domestic AC filters, with values of 4.69 × 103 cells/cm2 and 9.86 × 103 cells/cm2 for bacteria and fungi, respectively. Previous studies showed that culturable bacteria/fungi loading on HVAC filters in Beijing office buildings were 46–232 CFU/cm2 and 32–221 CFU/cm2, respectively, without cleaning for two years (Table S3). Luhung found a high concentration of microbial contamination on HVAC secondary filters (MERV 8 rating) with machine operation for 3–6 months.6 Noris et al. (2011) reported 1.1 × 106 CFU/g of bacteria collecting dust samples from HVAC filters in residences in the U.S..4 However, the current studies conducted a culture-independent approach, resulting in poor comparison of bacterial counts by the culture-dependent approach.

A total of 1,020,097 high-quality sequence reads were obtained from six filters of four households except for SH4, as the concentration of PCR amplification products failed to meet the sequencing requirements. The highest α-diversity index was observed in SH7, with values of 4.41 for Shannon and 0.042 for Simpson (Table S2). The results Chao1 showed that SH1 (911.00) had the highest richness, followed by SH7 (804.58) and SH2 (609.91). Notably, the bacterial concentration showed a trend similar to that of the Chao1 index, as observed in Figure 1b, suggesting that high-concentration contaminations in AC filters had higher bacterial-related community richness.

Regarding the bacteria community structure (Figure 1c,d), Proteobacteria were the most prevalent bacterial phyla across all the samples, accounting for 30.15%–40.80%, owing to better adaptability by possessing genes involving resistance to oxidative damage and desiccation.26 The Firmicutes (7.83% to 41.47%) and Actinobacteria (11.00% to 25.98%) were another two abundant taxons. The order of bacterial phylum is consistent with an indoor bioaerosol study, indicating the close link with indoor airborne microbiota.27 These three bacteria phylum were reported to represent 96% of the clones on the residential filters in the previous study.4 It was notable that Cyanobacteria were detected, of which the relative abundance fluctuated between 1.51% and 18.20%. Cyanobacteria can be suspended in the air by aqueous bubbles and wave bursts when the algal bloom occurs.28 The city near the coastal zone is highly likely subjected to airborne algae. The aerosolized cyanobacterial toxins may pose a threat to human health.29

Bacterial percentages varied significantly across samples at the genus level (Figure 1d). Streptococcus is associated with facultatively anaerobic and stress tolerance, dominating in F1, with values of 16.04% and 20.92% in SH1 and SH2, respectively. Lactobacillus was the most detected genus in F4 (27.38% and 20.30% in SH6 and SH7, respectively). Lactobacillus is a probiotic genus widely employed to prevent caries, diarrhea, and atopic dermatitis conducive to the digestive and immune systems, which was also found in dormitory and household rooms in the USA, closely related to human activities.30 Their phenotypes were mainly associated with facultatively anaerobic, Gram-positive, mobile elements, and were stress-tolerant (as shown in Figure 2). Moreover, Paracoccus, Corynebacterium, and Staphylococcus, whose phenotypes were facultatively anaerobic, were found across all samples (all relative abundance >1.00%). Another noticeable point was that the relative abundance of the various categories varied and clustered into three groups, which implied that the building occupants are responsible for shaping the bacterial community (Figure 1d). Human skin, mucous membranes, and intestines are primary sources for releasing bioaerosol. These bacterial genera, including Enhydrobacter, Micrococcus, Staphylococcus, Streptococcus, Haemophilus, etc., were often found indoors (Table S3), especially in residential households. Other genera, such as Paracoccus and Corynebacterium, which are prevalent in soil and water and ubiquitous throughout the environment, were also discovered.31,32 These genera may mainly originate from outdoor air. Bacterial phenotypes based on BugBase are mainly associated with aerobic, forming biofilms, and are stress tolerant (Figure 2). It indicated that the installation location of the filters was more conducive to the proliferation of aerobic bacteria, and these bacteria behaved as resilient and environmentally resistant. In short, maintaining clean and hygienic primary AC filters can significantly improve indoor air quality and safety.

Figure 2.

Figure 2

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Microbial community phenotypes and the corresponding bacterial contributions in different families were analyzed by BugBase based on the Order level. F1, F2, F3, and F4 represent different families.

3.2. Fungal Concentration, Community Structures, and Morphology Features

For fungi, the concentrations varied significantly, ranging from 1 × 103 to 1 × 107 copies/cm2 (Figure 3a). The dirtiest one (SH7) contained the highest concentration of fungal copy number (1.34 × 107 copies/cm2), while SH4 was relatively clean (1.00 × 103 copies/cm2). The concentrations of the ITS gene in most samples were considerably higher than those of the 16S rRNA gene. HVAC filters loaded plentiful fungi; however, house dust loaded more bacteria.33 This may result from the ambient temperature and humidity in indoor AC conditions. During the summer, when air conditioners are operating, AC systems often have high humidity, which may promote fungus growth. The lowest α-diversity was found in SH7, with values of 1.73 for the Shannon index and 0.289 for the Simpson index (Table S2). Higher Chao1 of SH1 (883.26) and SH2 (746.92) represented higher species richness in F1, while the dirtiest sample SH7 (Chao1:121.46) was the lowest (Figure 3a), indicating different levels of bacterial and fungal contamination on the AC filters might lead to a distinct trend of their richness or diversity (Figure 1b and Figure 3a).

Figure 3.

Figure 3

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(a) Concentrations (log10 copies/cm2) of fungi and fungal Chao index for seven filters from each family using qPCR tests. (b) Relative abundances of fungal genera. (c-l) Microscopic images from the filter dust suspension of samples SH1 and SH7 in Shanghai.

Ascomycota (94.47% ± 6.1%), whose ascospores were generally smaller than 2.5 μm and could be easily aerosolized,34 was much more abundant than Basidiomycota (5.31% ± 5.8%), which is used for food fermentation and medical treatment and acts as pathogens for some animal, plant, and human beings. Overall, the fungal compositions at the genus level were similar among the four households, but their relative abundances were significantly varied across the samples (Figure 3b). Aspergillus and Cladosporium were the most abundant fungal genera for most samples, except for SH3. Interestingly, SH7 (Figure 3a), with the highest fungal concentration, was overwhelmingly dominated by the Aspergillus and its relative abundance was up to 99.42% (Figure 3b). Aspergillus is present worldwide in a variety of confined environments, including primary and secondary air conditioning filters, indoor air, taxis, and personal automotive air conditioning filters in Brazil and Chinese cities (Table S3).15,35Aspergillus have a capacity for colonization on AC filter, leading to the proliferation of Aspergillus and the demise of others. Prior research proved that indoor dust contains nutrients to sustain microbial growth. Bakker et al. found a lower richness in air conditioning cooling coils due to high enrichment of specific microbial proliferation.8 Li et al. investigated the growth of microorganisms in air conditioning ducts and found that microorganisms developed well at temperatures between 22 °C and 32 °C and relative humidity between 40% and 90%, with a positive link between temperature and humidity increases.36 Additionally, recent research in several nations proved that Aspergillus is more prevalent at low latitudes in indoor environments, which was in line with our findings.37

Many biological particles, including the entire fungal cell structure, were observed through microscopic methods (Figure 3c–l). By referring to the fungal atlas and high-throughput sequencing results, we speculated on the fungus genus and the description of morphology. Alternaria was presumably observed in Figure 3d,e, characterized by rodlike or obclavate dictyoconidia multicellular and darkly pigmented spores with transverse and longitudinal septa and an apparent short conical or cylindrical beak at the tips.38 There was a refractive attachment scar at the tip of the beak. Cells in Figure 3c,f displayed similar ovoid shapes with a slightly curved phragmoconidia feature that the third part occupied the whole area, sympodial, pale brown, cylindrical, speculated as Curvularia. Bipolaris was observed in Figure 3g, which features sympodial growth of light brown, fusiform to ellipsoidal, pseudoseptate, and poroconidia on a geniculate or zigzag rachis.39 Conidia of Cladosporium species, which were nonseptate and have a smooth wall as shown in Figure 3i,40 are the most common airborne spores both indoors or outdoors, known to be allergenic and could infect immune-comprised individuals. Figure 3k is most likely microalgal microbes of the Chlorophyta, the most abundant group of microalgae, with about 90% living in freshwater.

3.3. Diversities and Community Structures of Pollen in AC Filters

Airborne pollen started attracting attention due to the ubiquitous existence of indoor and outdoor air, while few studies were conducted on pollen distribution on AC filters.41−44Figure 4 depicts pollen species on the AC filters. Compared to the bacteria and fungi community, less diversity in the pollen community was observed, as shown in Table S2. The Shannon index was 2.05 and 2.30 in SH6 and SH7, which were far higher than those of SH1, SH2, and SH5 (corresponding to 0.85, 0.75, and 0.57). Streptophyta was the most abundant phylum for all domestic filters (Figure 4a). At the genus level, Humulus (affiliation to the Magnoliopsida) was the most prevalent genus for all AC filters, with relative abundances ranging from 32.50% (SH6) to 89.75% (SH5) and an average value of 67.84%, followed by Boehmeria (SH7 0.98%–SH6 31.45%) and a mean value of 12.55% (Figure 4c). The suspended pollens would also be detrimental to indoor air quality.45 The anemophilous flower pollens were dominant because of smaller cell size compared to the entomophilous flower.46Humulus is a perennial herb and typical anemophily grass, widespread in most areas of China. It has a flowering period between August and October each year.47 Lu et al. (2020) proved that the proteins from Humulus pollen could cause an allergic response by Western blotting.47 The second abundant genus, Boehmeria, grows in tropical and subtropical areas in China and is used for producing superior long fibers.48 Their distribution in AC filters might originate from natural plants or human-associated uses.

Figure 4.

Figure 4

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Relative abundances of pollen (a) phylum, (b) order, and (c) genera of samples in Shanghai.

3.4. Potentially Pathogenic Microbes on AC Filters

Potential pathogens dominated by Rhizobiales, Acetobacterales, Staphylococcales, Burkholderiales, and others were determined by BugBase (as shown in Figure 2) to conduct a more in-depth investigation of human health (Figure S1). Nevertheless, the relative abundance varied significantly, suggesting that the ambient surroundings or human behaviors shaped the pathogenic bacteria community. F1 was heavily contaminated by Streptococcus, with a relative abundance of 18.48%, while Allorhizobium occupied 9.46% in F2, which was 44 times higher than that in F1 (0.21%). F1 and F3 held a high relative abundance of Staphylococcus (5.72% and 5.14%, respectively) and Corynebacterium (4.37% and 10.25%, respectively). Neisseria, a commensal and pathogenic resident of the human oropharynx, especially N. meningitidis and N.gonorrheae, was detected in F1 (3.08%), F3 (0.19%), and F4 (0.56%).49Haemophilus was observed in exclusive F1 (4.31%) and F4 (0.78%). The main species of Haemophilus is H. parainfluenzae, potentially causing urethritis, occasional cases of bacterial endocarditis, upper respiratory tract infections, sepsis, and biliary tract infections.50

Regarding the potentially pathogenic or allergenic fungi, studies have assessed that susceptible populations would be subjected to a respiratory health risk under the increased exposure to these indoor fungi.51 The predominant potential pathogenic fungi were Aspergillus, Cladosporium, Nigosora, and Alternaria. Specifically, Aspergillus penicillioides represented the predominant species, with proportions of 24.74%, 10.41%, 35.08%, and 53.41%, corresponding to F1, F2, F3, and F4, respectively. Aspergillus penicillioides is one of the most xerophilic indoor molds,52 and frequently found in residential dust. A. penicillioides could infect humans and cause lobomycosis.53 The Cladosporium halotolerans were the dominant species of Cladosporium, ranging from 0.02% to 21.89%, representing a clinical fungus in the USA.54 Direct human emissions, such as skin shedding, may also be a factor for obligate skin fungus. Dannemiller et al. found that Malassezia, a fungus that lives on human skin, was one of the most common taxa in house dust, causing diseases such as folliculitis, pityriasis vulgaris, and seborrheic dermatitis.55

4. Conclusion

This investigation demonstrated that AC filters carried a substantial quantity of microorganisms. The concentration, richness, diversity, and taxa of bacteria, fungi, and pollens were impacted by the frequency of air conditioning usage and cleaning of household users. Potentially pathogenic germs such as Staphylococcus, Streptococcus, Corynebacterium, Neisseria, and Haemophilus etc., were human-related genera among the top 20 bacteria, indicating that human occupants might be the major source of bacteria. The higher bacterial concentration determined a higher richness, whereas this pattern did not fit with fungus due to Aspergillus thriving, while other species perished in dirty samples. This genus was detected in great abundance and simultaneously acted as a potential pathogen. We also found abundant pollens carried by AC filters, dominated by Streptophyta at phylum. Humulus and Boehmeria were abundant genera, which would result in infection and allergic potentials. Overall, our work offers biologically based monitoring and insightful guidance for a better understanding of indoor biocontaminants exposure, which would help to safeguard the health of residential building environments.

Acknowledgments

This work was supported by the Ministry of Science and Technology of China (No. 2023YFC3708203). Daikin Industrial Co., LTD (No. 2021-01888), Science & Technology Commission of Shanghai Municipality (No. 21DZ1202300), Shanghai International Science and Technology Partnership Project (No.21230780200).

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/envhealth.3c00145.

  • Detailed materials and methods, comparison of microbiota in AC filters from different locations, heatmap analysis of potentially pathogenic bacteria and fungi (PDF)

Author Contributions

Xueyun Geng: conceptualization, methodology, formal analysis, methodology, writing–original draft. Changliang Nie: software, supervision, writing–review and editing. Lina Wang: supervision, writing–review and editing. Ling Li: supervision, writing–review and editing. Dan Li: writing–review and editing. Atsushi Nishino: supervision, writing–review and editing. Jianmin Chen: supervision, writing–review and editing, and funding acquisition. All of the authors were involved in the writing review and approved the final version of the manuscript.

The authors declare no competing financial interest.

Supplementary Material

eh3c00145_si_001.pdf (518.4KB, pdf)

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