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Downloaded with the Refseq Accessions Using E-Utilities Available BE Studies Conducted 16S Rrna Amplicon Se- on 2018-01-27 Merino et al. BMC Genomics (2019) 20:92 https://doi.org/10.1186/s12864-018-5389-z RESEARCH ARTICLE Open Access Comparative genomics of Bacteria commonly identified in the built environment Nancy Merino1,2, Shu Zhang3,4, Masaru Tomita5,6 and Haruo Suzuki5,6* Abstract Background: The microbial community of the built environment (BE) can impact the lives of people and has been studied for a variety of indoor, outdoor, underground, and extreme locations. Thus far, these microorganisms have mainly been investigated by culture-based methods or amplicon sequencing. However, both methods have limitations, complicating multi-study comparisons and limiting the knowledge gained regarding in-situ microbial lifestyles. A greater understanding of BE microorganisms can be achieved through basic information derived from the complete genome. Here, we investigate the level of diversity and genomic features (genome size, GC content, replication strand skew, and codon usage bias) from complete genomes of bacteria commonly identified in the BE, providing a first step towards understanding these bacterial lifestyles. Results: Here, we selected bacterial genera commonly identified in the BE (or “Common BE genomes”)andcompared them against other prokaryotic genera (“Other genomes”). The “Common BE genomes” were identified in various climates and in indoor, outdoor, underground, or extreme built environments. The diversity level of the 16S rRNA varied greatly between genera. The genome size, GC content and GC skew strength of the “Common BE genomes” were statistically larger than those of the “Other genomes” but were not practically significant. In contrast, the strength of selected codon usage bias (S value) was statistically higher with a large effect size in the “Common BE genomes” compared to the “Other genomes.” Conclusion: Of the four genomic features tested, the S value could play a more important role in understanding the lifestyles of bacteria living in the BE. This parameter could be indicative of bacterial growth rates, gene expression, and other factors, potentially affected by BE growth conditions (e.g., temperature, humidity, and nutrients). However, further experimental evidence, species-level BE studies, and classification by BE location is needed to define the relationship between genomic features and the lifestyles of BE bacteria more robustly. Keywords: Built environment, Bacteria, Diversity, Genomic features, Genome size, GC content, Replication strand skew, Codon usage bias Background to increase to 66% [2]. Moreover, people spend about The microbial community of the built environment (BE) 87% of their time indoors and about 6% in cars [3], sug- is an important player in human-microbe interactions. gesting that the indoor microbial community can play As such, in order to build urban environments that an important role in the lives of individuals. In fact, the benefit human well-being, it is necessary to study the re- indoor microbial community has already been shown to lationship between the BE and microbial communities. affect occupant health (e.g., respiratory health [4] and As of 2016, about 54% of the world’s population is living asthma [5]), including adverse effects on mental health in urban areas [1], and by 2050, this number is expected [6], and can be influenced by building design (e.g., venti- lation), occupants, and usage [7–9]. In turn, individuals can easily influence the surrounding microbial commu- * Correspondence: [email protected] 5Faculty of Environment and Information Studies, Keio University, Fujisawa, nity with their own personal microbiome, especially Kanagawa 252-0882, Japan through physical contact [10–12] and movement [13], 6 Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata leaving a microbial fingerprint in the built environment 997-0035, Japan Full list of author information is available at the end of the article [9, 14, 15]. The microbial community of the BE also © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Merino et al. BMC Genomics (2019) 20:92 Page 2 of 17 extends to the outdoor (e.g., green roofs [16] and parks genomes of the vaginal species were smaller with [17]), underground (e.g., transit systems [18–20]), and lower GC (guanine and cytosine) content compared extreme environments (e.g., cleanrooms [21]and to the non-vaginal species [56]. The observed genome space [21, 22]). size reduction suggests that the vaginal Lactobacillus The BE microbiome is slightly influenced by environ- species has “some degree of adaptation to a mental conditions, mainly temperature, humidity, and host-dependent lifestyle” and is commonly observed lighting [23–28]. Several other building parameters have in symbiotic microorganisms [56]. However, the indi- been tested previously (e.g., room pressure, CO2 concen- vidual organismal genome information (e.g., genome tration, surface material) but were not found to play a size and nucleotide composition) has not been inves- significant role in the microbial community composition tigated in depth for microorganisms in the BE. [29, 30]. Moisture levels are widely known to affect mi- In the present study, we performed genome sequence crobial abundances and activity, especially when water analyses for bacteria that have been commonly identified damage occurs (e.g., flooded homes had higher abun- in BEs, and focused on genomic features, including gen- dances of Penicillium [31]). However, many indoor built ome size, GC content, replication strand skew, and environments are largely devoid of water and nutrients, codon usage bias. This information could be useful for and it is likely that geographical location, on the scale of the characterization of the microbial members present cities or even at larger scales [32], plays a more import- in BEs, and in the future, these basic features might be ant role in the microbiome composition [30]. useful to help predict the microorganisms likely to adapt The relationship between humans and microorganisms to BE conditions. in the BE has moved from investigations limited to culture-based methods to approaches involving next- generation sequencing. One of the first publications on Results an indoor microbial community occurred in 1887 [33], Bacteria commonly identified in the built environment which expounded a positive correlation between the Built environments (BEs) are occupied by various micro- presence of indoor microorganisms and death rate. Since organisms and are also important transitions that link the advent of high-throughput sequencing, several stud- the natural world, humans, and the urban environment. ies have used amplicon sequencing to gain more infor- The indoor microbiome has already been shown to in- mation about the microbial community of the BE, fluence human health [4–6], and a building’s design and including the ribosomal RNA region (e.g., 16S rRNA) operation can play a major role in the spread of micro- for Bacteria and Archaea and the internal transcribed organisms, including pathogens [25]. For example, air spacer (ITS) region for Fungi [29]. The microbial com- and water via ventilation and plumbing systems, respect- munities of a variety of locations have been analyzed, ively, are major routes for microbial dispersal through- such as clean rooms [21], operating rooms [34], plumb- out a BE [25]. Since BEs are designed to improve the ing systems [35], universities [36], and transit systems lives of the individuals cohabiting them, it is important [18–20]. While these studies have enhanced our under- to understand the relationship between the BEs and the standing of the relationship between humans, microor- microorganisms therein. ganisms, and the built environment [25, 29, 37], there In this study, we selected 28 bacterial genera that are limitations to amplicon sequencing, including bias have been commonly identified in the BE at the gen- with sequencing primers, targeted amplicon region, era level from 54 publications (Additional file 1: DNA extraction protocols, and sequencing platforms Table S1–S2), ranging from various locations around [38], which make multi-study comparisons difficult. the world (Additional file 2: Figure S1) and covering Improving our understanding of microbial commu- four major BE locations (indoor, outdoor, under- nities in the BE can be achieved by analyzing draft or ground, and extreme), several sub-locations (e.g. hos- complete genomes derived from genomic and metage- pital, residential, recreation, space, subway, and nomic studies [39]. There have been several published cleanroom), climates, and 3 sample types (surface, genomes of bacteria collected from the BE, such as air, and water) (Table 1, Additional file 1:Table Dermacoccus nishinomiyaensis [40], Arthrobacter sp. S3-S5). The International Space Station (ISS) is in- [41], and Gordonia sp. [42], among others [43–53]. cluded as a built environment located in space (or These data provide detailed information on individual low Earth orbit), and the microorganisms
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