Effects of operational parameters on bacterial communities in Hong Kong and global wastewater treatment plants

ABSTRACT Wastewater treatment plants (WWTPs) are indispensable biotechnology facilities for modern cities and play an essential role in modern urban infrastructure by employing microorganisms to remove pollutants in wastewater, thus protecting public health and the environment. This study conducted a 13-month bacterial community survey of six full-scale WWTPs in Hong Kong with samples of influent, activated sludge (AS), and effluent to explore their synchronism and asynchronism of bacterial community. Besides, we compared AS results of six Hong Kong WWTPs with data from 1,186 AS amplicon data in 269 global WWTPs and a 9-year metagenomic sequencing survey of a Hong Kong WWTP. Our results showed the compositions of bacterial communities varied and the bacterial community structure of AS had obvious differences across Hong Kong WWTPs. The co-occurrence analysis identified 40 pairs of relationships that existed among Hong Kong WWTPs to show solid associations between two species and stochastic processes took large proportions for the bacterial community assembly of six WWTPs. The abundance and distribution of the functional bacteria in worldwide and Hong Kong WWTPs were examined and compared, and we found that ammonia-oxidizing bacteria had more diversity than nitrite-oxidizing bacteria. Besides, Hong Kong WWTPs could make great contributions to the genome mining of microbial dark matter in the global “wanted list.” Operational parameters had important effects on OTUs’ abundance, such as the temperature to the genera of Tetrasphaera, Gordonia and Nitrospira. All these results obtained from this study can deepen our understanding of the microbial ecology in WWTPs and provide foundations for further studies. IMPORTANCE Wastewater treatment plants (WWTPs) are an indispensable component of modern cities, as they can remove pollutants in wastewater to prevent anthropogenic activities. Activated sludge (AS) is a fundamental wastewater treatment process and it harbors a highly complex microbial community that forms the main components and contains functional groups. Unveiling “who is there” is a long-term goal of the research on AS microbiology. High-throughput sequencing provides insights into the inventory diversity of microbial communities to an unprecedented level of detail. At present, the analysis of communities in WWTPs usually comes from a specific WWTP and lacks comparisons and verification among different WWTPs. The wide-scale and long-term sampling project and research in this study could help us evaluate the AS community more accurately to find the similarities and different results for different WWTPs in Hong Kong and other regions of the world. Wastewater treatment plants (WWTPs) are an indispensable component of modern cities, as they can remove pollutants in wastewater to prevent anthropogenic activities. Activated sludge (AS) is a fundamental wastewater treatment process and it harbors a highly complex microbial community that forms the main components and contains functional groups. Unveiling “who is there” is a long-term goal of the research on AS microbiology. High-throughput sequencing provides insights into the inventory diversity of microbial communities to an unprecedented level of detail. At present, the analysis of communities in WWTPs usually comes from a specific WWTP and lacks comparisons and verification among different WWTPs. The wide-scale and long-term sampling project and research in this study could help us evaluate the AS community more accurately to find the similarities and different results for different WWTPs in Hong Kong and other regions of the world.

[1]  Chenxiang Sun,et al.  Differences in distributions, assembly mechanisms, and putative interactions of AOB and NOB at a large spatial scale , 2023, Frontiers of Environmental Science & Engineering.

[2]  T. Zhang,et al.  The microbial dark matter and “wanted list” in worldwide wastewater treatment plants , 2023, Microbiome.

[3]  Harris H. Wang,et al.  High-throughput microbial culturomics using automation and machine learning , 2023, Nature Biotechnology.

[4]  S. Lücker,et al.  Low diversity and microdiversity of comammox bacteria in wastewater systems suggest specific adaptations within the Ca. Nitrospira nitrosa cluster. , 2022, Water research.

[5]  P. Kämpfer,et al.  High diversity of the emerging pathogen Acinetobacter baumannii and other Acinetobacter spp. in raw manure, biogas plants digestates, and rural and urban wastewater treatment plants with system specific antimicrobial resistance profiles. , 2022, The Science of the total environment.

[6]  S. Petrovski,et al.  The phylogeny, ecology and ecophysiology of the glycogen accumulating organism (GAO) Defluviicoccus in wastewater treatment plants. , 2022, Water research.

[7]  Tong Zhang,et al.  Culturing the uncultured microbial majority in activated sludge: A critical review , 2022, Critical Reviews in Environmental Science and Technology.

[8]  Samir V. Deshpande,et al.  A ribosomal operon database and MegaBLAST settings for strain-level resolution of microbiomes. , 2022, FEMS microbes.

[9]  Tong Zhang,et al.  Charting the complexity of the activated sludge microbiome through a hybrid sequencing strategy , 2021, Microbiome.

[10]  Donovan H. Parks,et al.  Successional dynamics and alternative stable states in a saline activated sludge microbial community over 9 years , 2021, Microbiome.

[11]  T. Hübschmann,et al.  Community and single cell analyses reveal complex predatory interactions between bacteria in high diversity systems , 2021, Nature Communications.

[12]  Bryan M. Wong,et al.  Machine Learning: New Ideas and Tools in Environmental Science and Engineering. , 2021, Environmental science & technology.

[13]  T. Zhang,et al.  MiDAS 4: A global catalogue of full-length 16S rRNA gene sequences and taxonomy for studies of bacterial communities in wastewater treatment plants , 2021, Nature Communications.

[14]  M. Nierychlo,et al.  Low Global Diversity of Candidatus Microthrix, a Troublesome Filamentous Organism in Full-Scale WWTPs , 2021, Frontiers in Microbiology.

[15]  M. T. Angulo,et al.  Predicting microbiome compositions from species assemblages through deep learning , 2021, bioRxiv.

[16]  Jizhong Zhou,et al.  Seasonal dynamics of the microbial community in two full-scale wastewater treatment plants: Diversity, composition, phylogenetic group based assembly and co-occurrence pattern. , 2021, Water research.

[17]  Ryan J. Newton,et al.  Urban wastewater bacterial communities assemble into seasonal steady states , 2021, Microbiome.

[18]  E. Korzeniewska,et al.  Wastewater treatment plants as a reservoir of integrase and antibiotic resistance genes - An epidemiological threat to workers and environment. , 2021, Environment international.

[19]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[20]  S. Wuertz,et al.  Sustained organic loading disturbance favors nitrite accumulation in bioreactors with variable resistance, recovery and resilience of nitrification and nitrifiers , 2020, Scientific Reports.

[21]  V. de Crécy-Lagard,et al.  A network approach to elucidate and prioritize microbial dark matter in microbial communities , 2020, The ISME journal.

[22]  A. Arkin,et al.  A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming , 2020, Nature Communications.

[23]  M. Nierychlo,et al.  MiDAS 3: An ecosystem-specific reference database, taxonomy and knowledge platform for activated sludge and anaerobic digesters reveals species-level microbiome composition of activated sludge. , 2020, Water research.

[24]  Tong Zhang,et al.  Genome-centric microbiome analysis reveals solid retention time (SRT)-shaped species interactions and niche differentiation in food waste and sludge co-digesters. , 2020, Water research.

[25]  Xiao-yan Li,et al.  Specific and effective detection of anammox bacteria using PCR primers targeting the 16S rRNA gene and functional genes. , 2020, The Science of the total environment.

[26]  Donovan H. Parks,et al.  A complete domain-to-species taxonomy for Bacteria and Archaea , 2020, Nature Biotechnology.

[27]  Jizhong Zhou,et al.  The biogeography and assembly of microbial communities in wastewater treatment plants in China. , 2020, Environmental science & technology.

[28]  A. Texier,et al.  Biological ammonium and sulfide oxidation in a nitrifying sequencing batch reactor: Kinetic and microbial population dynamics assessments. , 2020, Chemosphere.

[29]  M. Nierychlo,et al.  Bacteria from the Genus Arcobacter Are Abundant in Effluent from Wastewater Treatment Plants , 2020, Applied and Environmental Microbiology.

[30]  Sheng Chang,et al.  Disentangling Community Structure of Ecological System in Activated Sludge: Core Communities, Functionality, and Functional Redundancy , 2020, Microbial Ecology.

[31]  Wen-Tso Liu,et al.  Machine learning-aided analyses of thousands of draft genomes reveal specific features of activated sludge processes , 2020, Microbiome.

[32]  Jizhong Zhou,et al.  Biodegradability of wastewater determines microbial assembly mechanisms in full-scale wastewater treatment plants. , 2019, Water research.

[33]  C. Médigue,et al.  MicroScope: an integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis , 2019, Nucleic Acids Res..

[34]  A. Isabwe,et al.  Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons , 2019, Microbiome.

[35]  B. Mamba,et al.  Diversity, Co-occurrence and Implications of Fungal Communities in Wastewater Treatment Plants , 2019, Scientific Reports.

[36]  D. Figeys,et al.  Exploring the effects of operational mode and microbial interactions on bacterial community assembly in a one-stage partial-nitritation anammox reactor using integrated multi-omics , 2019, Microbiome.

[37]  Yunpeng Liu,et al.  Diversity-triggered deterministic bacterial assembly constrains community functions , 2019, Nature Communications.

[38]  X. Hao,et al.  Research advances of Tetrasphaera in enhanced biological phosphorus removal: A review. , 2019, Water research.

[39]  Francesco Asnicar,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[40]  S. McIlroy,et al.  Generation of Comprehensive Ecosystem-Specific Reference Databases with Species-Level Resolution by High-Throughput Full-Length 16S rRNA Gene Sequencing and Automated Taxonomy Assignment (AutoTax) , 2019, mBio.

[41]  Daron M. Standley,et al.  MAFFT-DASH: integrated protein sequence and structural alignment , 2019, Nucleic Acids Res..

[42]  T. LaPara,et al.  Composition and Dynamics of the Activated Sludge Microbiome during Seasonal Nitrification Failure , 2019, Scientific Reports.

[43]  J. E. Weaver,et al.  Global diversity and biogeography of bacterial communities in wastewater treatment plants , 2019, Nature Microbiology.

[44]  Tong Zhang,et al.  Toward an Intensive Longitudinal Understanding of Activated Sludge Bacterial Assembly and Dynamics. , 2018, Environmental science & technology.

[45]  E. Alm,et al.  Interactions in self-assembled microbial communities saturate with diversity , 2018, The ISME Journal.

[46]  Michaeline B. N. Albright,et al.  Function and functional redundancy in microbial systems , 2018, Nature Ecology & Evolution.

[47]  M. Doebeli,et al.  Correcting for 16S rRNA gene copy numbers in microbiome surveys remains an unsolved problem , 2018, Microbiome.

[48]  M. Kuypers,et al.  The microbial nitrogen-cycling network , 2018, Nature Reviews Microbiology.

[49]  B. Smets,et al.  Density and distribution of nitrifying guilds in rapid sand filters for drinking water production: Dominance of Nitrospira spp. , 2017, Water research.

[50]  S. Littmann,et al.  Adaptability as the key to success for the ubiquitous marine nitrite oxidizer Nitrococcus , 2017, Science Advances.

[51]  Jizhong Zhou,et al.  Stochastic Community Assembly: Does It Matter in Microbial Ecology? , 2017, Microbiology and Molecular Biology Reviews.

[52]  M. Reis,et al.  Metabolism and ecological niche of Tetrasphaera and Ca. Accumulibacter in enhanced biological phosphorus removal. , 2017, Water research.

[53]  Donovan H. Parks,et al.  Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life , 2017, Nature Microbiology.

[54]  Tong Zhang,et al.  Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China , 2017, Microbiome.

[55]  Xudong Li,et al.  A review: Driving factors and regulation strategies of microbial community structure and dynamics in wastewater treatment systems. , 2017, Chemosphere.

[56]  G. Wells,et al.  Regional synchrony in full-scale activated sludge bioreactors due to deterministic microbial community assembly , 2016, The ISME Journal.

[57]  D. Frigon,et al.  Bacterial community assembly in activated sludge: mapping beta diversity across environmental variables , 2016, MicrobiologyOpen.

[58]  W. Waegeman,et al.  Absolute quantification of microbial taxon abundances , 2016, The ISME Journal.

[59]  Willy Verstraete,et al.  Perspectives for microbial community composition in anaerobic digestion: from abundance and activity to connectivity. , 2016, Environmental microbiology.

[60]  M. Wagner,et al.  A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria. , 2016, Trends in microbiology.

[61]  G. Tyson,et al.  Genome-centric resolution of microbial diversity, metabolism and interactions in anaerobic digestion. , 2016, Environmental microbiology.

[62]  P. Reich,et al.  Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning , 2016 .

[63]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[64]  Tong Zhang,et al.  Population Dynamics of Bulking and Foaming Bacteria in a Full-scale Wastewater Treatment Plant over Five Years , 2016, Scientific Reports.

[65]  Niels W. Hanson,et al.  Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems. , 2015, Environmental microbiology.

[66]  Aaron Marc Saunders,et al.  The activated sludge ecosystem contains a core community of abundant organisms , 2015, The ISME Journal.

[67]  M. Sogin,et al.  Sewage Reflects the Microbiomes of Human Populations , 2015, mBio.

[68]  Robert Hein,et al.  rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development , 2014, Nucleic Acids Res..

[69]  Tong Zhang,et al.  Bacterial assembly and temporal dynamics in activated sludge of a full-scale municipal wastewater treatment plant , 2014, The ISME Journal.

[70]  Michael Wagner,et al.  Nitrotoga-like bacteria are previously unrecognized key nitrite oxidizers in full-scale wastewater treatment plants , 2014, The ISME Journal.

[71]  Christian L. Müller,et al.  Sparse and Compositionally Robust Inference of Microbial Ecological Networks , 2014, PLoS Comput. Biol..

[72]  Natalia N. Ivanova,et al.  Insights into the phylogeny and coding potential of microbial dark matter , 2013, Nature.

[73]  F. Ibarbalz,et al.  Industrial activated sludge exhibit unique bacterial community composition at high taxonomic ranks. , 2013, Water research.

[74]  Thomas P. Curtis,et al.  Microbial community assembly, theory and rare functions , 2013, Front. Microbiol..

[75]  W. Wanek,et al.  Interactions of Nitrifying Bacteria and Heterotrophs: Identification of a Micavibrio-Like Putative Predator of Nitrospira spp , 2013, Applied and Environmental Microbiology.

[76]  G. Pusch,et al.  Phylogenetic conservatism of functional traits in microorganisms , 2012, The ISME Journal.

[77]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[78]  Aaron Marc Saunders,et al.  A metabolic model for members of the genus Tetrasphaera involved in enhanced biological phosphorus removal , 2012, The ISME Journal.

[79]  Aaron Marc Saunders,et al.  Microbial communities involved in enhanced biological phosphorus removal from wastewater--a model system in environmental biotechnology. , 2012, Current opinion in biotechnology.

[80]  Feng Luo,et al.  Molecular ecological network analyses , 2012, BMC Bioinformatics.

[81]  Tong Zhang,et al.  Profiling bulking and foaming bacteria in activated sludge by high throughput sequencing. , 2012, Water research.

[82]  Noah Fierer,et al.  Using network analysis to explore co-occurrence patterns in soil microbial communities , 2011, The ISME Journal.

[83]  Zhengqin Xiong,et al.  Autotrophic growth of nitrifying community in an agricultural soil , 2011, The ISME Journal.

[84]  Aaron Marc Saunders,et al.  A conceptual ecosystem model of microbial communities in enhanced biological phosphorus removal plants. , 2010, Water research.

[85]  Irina Dana Ofiteru,et al.  Combined niche and neutral effects in a microbial wastewater treatment community , 2010, Proceedings of the National Academy of Sciences.

[86]  Paramvir S. Dehal,et al.  FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments , 2010, PloS one.

[87]  Thomas L. Madden,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[88]  Mathieu Bastian,et al.  Gephi: An Open Source Software for Exploring and Manipulating Networks , 2009, ICWSM.

[89]  J. G. Kuenen,et al.  Anammox bacteria: from discovery to application , 2008, Nature Reviews Microbiology.

[90]  Debojyoti Dutta,et al.  Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors , 2006, Bioinform..

[91]  Daniel B. Oerther,et al.  Quantifying filamentous microorganisms in activated sludge before, during, and after an incident of foaming by oligonucleotide probe hybridizations and antibody staining. , 2001, Water research.

[92]  G. Dalhammar,et al.  Development of nitrification inhibition assays using pure cultures of Nitrosomonas and Nitrobacter. , 2001, Water research.

[93]  E. Jurkevitch,et al.  Bdellovibrio exovorus sp. nov., a novel predator of Caulobacter crescentus. , 2013, International journal of systematic and evolutionary microbiology.

[94]  J. Leeds.  Patterns and processes of microbial community assembly , 2013 .

[95]  M. C. Tomei,et al.  "Microthrix parvicella", a filamentous bacterium causing bulking and foaming in activated sludge systems: a review of current knowledge. , 2005, FEMS microbiology reviews.

[96]  Ben Nichols,et al.  Distributed under Creative Commons Cc-by 4.0 Vsearch: a Versatile Open Source Tool for Metagenomics , 2022 .