Socioeconomic drivers of the human microbiome footprint in global sewage

Minglei Ren , Shaojuan Du , Jianjun Wang

Front. Environ. Sci. Eng. ›› 2024, Vol. 18 ›› Issue (10) : 129

PDF (8840KB)
Front. Environ. Sci. Eng. ›› 2024, Vol. 18 ›› Issue (10) : 129 DOI: 10.1007/s11783-024-1889-z
RESEARCH ARTICLE

Socioeconomic drivers of the human microbiome footprint in global sewage

Author information +
History +
PDF (8840KB)

Abstract

● We built a read-mapping framework to profile human microbes from sewages (HSM).

● There were 95.03% human microbial species successfully recaptured from sewages.

● The HSM composition showed a distance-decay pattern at a global scale.

● The HSM communities from developed regions were separated from developing regions.

● Economy was the key socioeconomic factors driving the HSM diversity.

The human microbiome leaves a legacy in sewage ecosystems, also referred to as the human sewage microbiomes (HSM), and could cause potential risk to human health and ecosystem service. However, these host-associated communities remain understudied, especially at a global scale, regarding microbial diversity, community composition and the underlying drivers. Here, we built a metagenomic read mapping-based framework to estimate HSM abundance in 243 sewage samples from 60 countries across seven continents. Our approach revealed that 95.03% of human microbiome species were identified from global sewage, demonstrating the potential of sewage as a lens to explore these human-associated microbes while bypassing the limitations of human privacy concerns. We identified significant biogeographic patterns for the HSM community, with species richness increasing toward high latitudes and composition showing a distance-decay relationship at a global scale. Interestingly, the HSM communities were mainly clustered by continent, with those from Europe and North America being separated from Asia and Africa. Furthermore, global HSM diversity was shown to be shaped by both climate and socioeconomic variables. Specifically, the average annual temperature was identified as the most important factor for species richness (33.18%), whereas economic variables such as country export in goods and services contributed the most to the variation in community composition (27.53%). Economic and other socioeconomic variables, such as education, were demonstrated to have direct effects on the HSM, as indicated by structural equation modeling. Our study provides the global biogeography of human sewage microbiomes and highlights the economy as an important socioeconomic factor driving host-associated community composition.

Graphical abstract

Keywords

Human sewage microbiome / Biogeography / Socioeconomic factors / Climate factors

Cite this article

Download citation ▾
Minglei Ren, Shaojuan Du, Jianjun Wang. Socioeconomic drivers of the human microbiome footprint in global sewage. Front. Environ. Sci. Eng., 2024, 18(10): 129 DOI:10.1007/s11783-024-1889-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahn J, Hayes R B. (2021). Environmental influences on the human microbiome and implications for noncommunicable disease. Annual Review of Public Health, 42(1): 277–292

[2]

Amaruddin A I, Hamid F, Koopman J P R, Muhammad M, Brienen E A T, van Lieshout L, Geelen A R, Wahyuni S, Kuijper E J, Sartono E. . (2020). The bacterial gut microbiota of schoolchildren from high and low socioeconomic status: a study in an urban area of Makassar, Indonesia. Microorganisms, 8(6): 961

[3]

AndrewsS (2010). FastQC: a Quality Control Tool for High Throughput Sequence Data. Cambridge: Babraham Institute

[4]

Bastian S, M M. (2009). Gephi: an open source software for exploring and manipulating networks. Proceedings of the International AAAI Conference on Web and Social Media, 3(1): 361–362

[5]

Belstrøm D, Holmstrup P, Nielsen C H, Kirkby N, Twetman S, Heitmann B L, Klepac-Ceraj V, Paster B J, Fiehn N E (2014). Bacterial profiles of saliva in relation to diet, lifestyle factors, and socioeconomic status. Journal of Oral Microbiology, 6(1): 09

[6]

Bibby K, Viau E, Peccia J. (2010). Pyrosequencing of the 16S rRNA gene to reveal bacterial pathogen diversity in biosolids. Water Research, 44(14): 4252–4260

[7]

Bolger A M, Lohse M, Usadel B. (2014). Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics, 30(15): 2114–2120

[8]

Bowyer R C, Jackon M A, Le Roy C I, Lochlainn M N, Spector T D, Dowd J B, Steves C J. (2019). . , 7(1):

[9]

Bradley R H, Corwyn R F. (2002). Socioeconomic status and child development. Annual Review of Psychology, 53(1): 371–399

[10]

Cai L, Ju F, Zhang T. (2014). Tracking human sewage microbiome in a municipal wastewater treatment plant. Applied Microbiology and Biotechnology, 98(7): 3317–3326

[11]

Catania F, Baedke J, Fábregas-Tejeda A, Nieves Delgado A, Vitali V, Long L A N. (2021). Global climate change, diet, and the complex relationship between human host and microbiome: towards an integrated picture. BioEssays, 43(6): 2100049

[12]

Chen X, Chen X, Zhao Y, Zhou H, Xiong X, Wu C. (2020). Effects of microplastic biofilms on nutrient cycling in simulated freshwater systems. Science of the Total Environment, 719: 137276

[13]

Crits-Christoph A, Kantor R S, Olm M R, Whitney O N, Al-Shayeb B, Lou Y C, Flamholz A, Kennedy L C, Greenwald H, Hinkle A J. (2020). . ,

[14]

Deschasaux M, Bouter K E, Prodan A, Levin E, Groen A K, Herrema H, Tremaroli V, Bakker G J, Attaye I, Pinto-Sietsma S J. . (2018). Depicting the composition of gut microbiota in a population with varied ethnic origins but shared geography. Nature Medicine, 24(10): 1526–1531

[15]

DixonP (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14: 927-930

[16]

Dowd J B, Renson A. (2018). “Under the skin” and into the gut: social epidemiology of the microbiome. Current Epidemiology Reports, 5(4): 432–441

[17]

Eren A M, Sogin M L, Morrison H G, Vineis J H, Fisher J C, Newton R J, McLellan S L. (2015). A single genus in the gut microbiome reflects host preference and specificity. ISME Journal, 9(1): 90–100

[18]

García-Aljaro C, Blanch A R, Campos C, Jofre J, Lucena F. (2019). Pathogens, faecal indicators and human-specific microbial source-tracking markers in sewage. Journal of Applied Microbiology, 126(3): 701–717

[19]

Gudda F O, Waigi M G, Odinga E S, Yang B, Carter L, Gao Y. (2020). Antibiotic-contaminated wastewater irrigated vegetables pose resistance selection risks to the gut microbiome. Environmental Pollution, 264: 114752

[20]

Gunawan W B, Abadi M N P, Fadhillah F S, Nurkolis F, Pramono A. (2023). The interlink between climate changes, gut microbiota, and aging processes. Human Nutrition & Metabolism, 32: 200193

[21]

Hendriksen R S, Munk P, Njage P, van Bunnik B, McNally L, Lukjancenko O, Röder T, Nieuwenhuijse D, Pedersen S K, Kjeldgaard J. . (2019). Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nature Communications, 10(1): 1124

[22]

Hijmans J, R S E, Cameron J L, Parra P G, Jones A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25: 1965–1978

[23]

Hu J, A H, Wang B, Sun G, Niu J, Si C, Wang X, Yeh X, Zhu J. . (2020). Mountain biodiversity and ecosystem functions: interplay between geology and contemporary environments. ISME Journal, 14: 1–14

[24]

Ji M, Liu Z, Sun K, Li Z, Fan X, Li Q. (2021). Bacteriophages in water pollution control: advantages and limitations. Frontiers of Environmental Science & Engineering, 15(5): 84

[25]

Jones E R, van Vliet M T H, Qadir M, Bierkens M F P. (2021). Country-level and gridded estimates of wastewater production, collection, treatment and reuse. Earth System Science Data, 13(2): 237–254

[26]

LaMartina E L, Mohaimani A A, Newton R J. (2021). Urban wastewater bacterial communities assemble into seasonal steady states. Microbiome, 9(1): 116

[27]

Langmead B, Salzberg S L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357–359

[28]

Li B, Ju F, Cai L, Zhang T. (2015). Profile and fate of bacterial pathogens in sewage treatment plants revealed by high-throughput metagenomic approach. Environmental Science & Technology, 49(17): 10492–10502

[29]

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078–2079

[30]

Li M, Song G, Liu R, Huang X, Liu H. (2022). Inactivation and risk control of pathogenic microorganisms in municipal sludge treatment: a review. Frontiers of Environmental Science & Engineering, 16(6): 70

[31]

Martínez I, Stegen J C, Maldonado-Gómez M X, Eren A M, Siba P M, Greenhill A R, Walter J. (2015). The gut microbiota of rural Papua New Guineans: composition, diversity patterns, and ecological processes. Cell Reports, 11(4): 527–538

[32]

Mateo-Sagasta J, Raschid-sally L, Thebo A (2015). Global wastewater and sludge production, treatment and use. In: Drechsel P, Qadir M, Wichelns D, eds. Wastewater. Dordrecht: Springer

[33]

Matus M, Duvallet C, Soule M K, Kearney S M, Endo N, Ghaeli N, Brito I, Ratti C, Kujawinski E B, Alm E J. (2019). . ,

[34]

Miller G E, Engen P A, Gillevet P M, Shaikh M, Sikaroodi M, Forsyth C B, Mutlu E, Keshavarzian A. (2016). Lower neighborhood socioeconomic status associated with reduced diversity of the colonic microbiota in healthy adults. PLoS One, 11(2): e0148952

[35]

Nadimpalli M L, Marks S J, Montealegre M C, Gilman R H, Pajuelo M J, Saito M, Tsukayama P, Njenga S M, Kiiru J, Swarthout J. . (2020). Urban informal settlements as hotspots of antimicrobial resistance and the need to curb environmental transmission. Nature Microbiology, 5(6): 787–795

[36]

Newton R J, Mclellan S, Dila D K, Vineis J H, Morrison H G, Eren A M, Sogin M L. (2015). Sewage reflects the microbiomes of human populations. mBio, 6(2): e02574

[37]

Nowak P, Troseid M, Avershina E, Barqasho B, Neogi U, Holm K, Hov J R, Noyan K, Vesterbacka J, Svärd J. . (2015). Gut microbiota diversity predicts immune status in HIV-1 infection. AIDS, 29(18): 2409–2418

[38]

Nowrotek M, Jałowiecki Ł, Harnisz M, Płaza G A. (2019). Culturomics and metagenomics: in understanding of environmental resistome. Frontiers of Environmental Science & Engineering, 13: 40

[39]

Parizadeh M, Arrieta M C. (2023). The global human gut microbiome: genes, lifestyles, and diet. Trends in Molecular Medicine, 29(10): 789–801

[40]

Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F, Beghini F, Manghi P, Tett A, Ghensi P. . (2019). Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell, 176(3): 649–662.e20

[41]

Pipek O A, Medgyes-Horváth A, Dobos L, Stéger J, Szalai-Gindl J, Visontai D, Kaas R S, Koopmans M, Hendriksen R S, Aarestrup F M. . (2019). Worldwide human mitochondrial haplogroup distribution from urban sewage. Scientific Reports, 9(1): 11624

[42]

Qin J, Li R, Raes J, Arumugam M, Burgdorf K S, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T J. . (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464(7285): 59–65

[43]

Schneeberger P H H, Fuhrimann S, Becker S L, Pothier J F, Duffy B, Beuret C, Frey J E, Utzinger J. (2019). Qualitative microbiome profiling along a wastewater system in Kampala, Uganda. Scientific Reports, 9(1): 17334

[44]

Sidhu J P S, Hodgers L, Ahmed W, Chong M N, Toze S. (2012). Prevalence of human pathogens and indicators in stormwater runoff in Brisbane, Australia. Water Research, 46(20): 6652–6660

[45]

Staley C, Reckhow K H, Lukasik J, Harwood V J. (2012). Assessment of sources of human pathogens and fecal contamination in a Florida freshwater lake. Water Research, 46(17): 5799–5812

[46]

Tisza M, Javornik C S, Avadhanula V, Zhang P, Ayvaz T, Feliz K, Hoffman K L, Clark J R, Terwilliger A, Ross M C. . (2023). Wastewater sequencing reveals community and variant dynamics of the collective human virome. Nature Communications, 14(1): 6878

[47]

Tiwari A, Krolicka A, Tran T T, Räisänen K, Ásmundsdóttir Á M, Wikmark O G, Lood R, Pitkänen T. (2024). Antibiotic resistance monitoring in wastewater in the Nordic countries: a systematic review. Environmental Research, 246: 118052

[48]

Wu L, Ning D, Zhang B, Li Y, Zhang P, Shan X, Zhang Q, Brown M R, Li Z, Van Nostrand J D. . (2019). Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nature Microbiology, 4(7): 1183–1195

[49]

Yatsunenko T, Rey F E, Manary M J, Trehan I, Dominguez-Bello M G, Contreras M, Magris M, Hidalgo G, Baldassano R N, Anokhin A P. (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402): 222–227

[50]

Zhao J, Li B, Lv P, Hou J, Qiu Y, Huang X. (2022). Distribution of antibiotic resistance genes and their association with bacteria and viruses in decentralized sewage treatment facilities. Frontiers of Environmental Science & Engineering, 16(3): 35

RIGHTS & PERMISSIONS

Higher Education Press 2024

AI Summary AI Mindmap
PDF (8840KB)

Supplementary files

FSE-24075-OF-RML_suppl_1

1517

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/