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  • 1.
    Hu, Yue
    KTH, School of Biotechnology (BIO).
    Microbial DNA Sequencing in Environmental Studies2017Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The field of microbial ecology has just entered a new era of rapid technological development and generation of big data. The high-throughput sequencing techniques presently available provide an opportunity to extensively inventorize the blueprints of life. Now, millions of microbes of natural microbial communities can be studied simultaneously without prior cultivation. New species and new functions (genes) can be discovered just by mining sequencing data. However, there is still a tremendous number of microorganisms not yet examined, nor are the ecosystem functions these carry out. The modern genomic technologies can contribute to solve environmental problems and help us understand ecosystems, but to most efficiently do so, methods need to be continuously optimised.

     

    During my Ph. D. studies, I developed a method to survey eukaryotic microbial diversity with a higher accuracy, and applied various sequencing-based approaches in an attempt to answer questions of importance in environmental research and ecology. In PAPER-I, we developed a set of 18S rRNA gene PCR primers with high taxonomic coverage, meeting the requirements of currently popular sequencing technologies and matching the richness of 18S rRNA reference sequences accumulated so far. In PAPER-II, we conducted the first sequencing-based spatial survey on the combined eukaryotic and bacterial planktonic community in the Baltic Sea to uncover the relationship of microbial diversity and environmental conditions. Here, the 18S primers designed in PAPER-I and a pair of broad-coverage 16S primers were employed to target the rRNA genes of protists and bacterioplankton for amplicon sequencing. In PAPER-III, we integrated metagenomic, metabarcoding, and metatranscriptomic data in an effort to scrutinise the protein synthesis potential (i.e., activity) of microbes in the sediment at a depth of 460 m in the Baltic Sea and, thus, disclosing microbial diversity and their possible ecological functions within such an extreme environment. Lastly, in PAPER-IV, we compared the performance of E. coli culturing, high-throughput sequencing, and portable real-time sequencing in tracking wastewater contamination in an urban stormwater system. From the aspects of cost, mobility and accuracy, we evaluated the usage of sequencing-based approaches in civil engineering, and for the first time, validated the real-time sequencing device in use within water quality monitoring.

     

    In summary, these studies demonstrate how DNA sequencing of microbial communities can be applied in environmental monitoring and ecological research.

  • 2.
    Hu, Yue
    et al.
    KTH, School of Biotechnology (BIO).
    Ndegwa, Nelson
    Karolinska Institutet, Department of Medical Epidemiology and Biostatistics (MEB).
    Alneberg, Johannes
    KTH, School of Biotechnology (BIO).
    Johansson, Sebastian
    KTH, School of Biotechnology (BIO).
    Logue, Jürg
    Linnaeus University, Centre for Ecology and Evolution in Microbial Model Systems.
    Huss, Mikael
    Stockholm University.
    Käller, Max
    KTH, School of Biotechnology (BIO).
    Lundeberg, Joakim
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Fagerberg, Jens
    Stockholm Vatten och Avfall AB.
    Andersson, Anders
    KTH, School of Biotechnology (BIO).
    Stationary and portable sequencing-based approaches for tracing wastewater contamination in urban stormwater systemsManuscript (preprint) (Other academic)
    Abstract [en]

    Urban sewer systems consist of wastewater and stormwater sewers, of which typically only

    the wastewater is processed before being discharged. Occasionally, misconnections or

    damages in the network occur, resulting in wastewater entering the stormwater system and

    being discharged without prior processing. Cultivation of faecal indicator bacteria, such as

    Escherichia coli (E. coli), is the current standard for tracing wastewater contamination. This

    method is cheap but cannot be employed in the field and is characterised by its limited

    specificity. Here, we compared the E. coli culturing approach with two different DNA

    sequencing-based methodologies (i.e., 16S rRNA amplicon sequencing on the Illumina

    MiSeq platform and shotgun metagenomic sequencing on an Oxford Nanopore MinIOn

    device), analysing 73 stormwater samples collected throughout the Stockholm city areas.

    High correlations were obtained between E. coli culturing counts and frequencies of human

    gut microbiome sequencing reads (via amplicon sequencing), indicating that E. coli is indeed

    a good indicator of faecal contamination. In contrast to E.coli culturing, amplicon sequencing

    could, however, further distinguish between two different sources of contamination in an

    area, where misconnections in the stormwater system were later on detected. Shotgun

    metagenomic sequencing on a subset of the samples using the portable Oxford Nanopore

    MinION real-time sequencing device correlated well with the amplicon sequencing data. In

    summary, this study shows that DNA sequencing allows distinguishing different

    contamination sources in stormwater systems and demonstrates the potential of using a

    portable sequencing device in the field for tracking faecal contamination.

  • 3.
    Hu, Yue O. O.
    et al.
    KTH, Centres, Science for Life Laboratory, SciLifeLab. KTH, School of Biotechnology (BIO), Gene Technology.
    Karlson, Bengt
    Charvet, Sophie
    Andersson, Anders F.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Diversity of Pico- to Mesoplankton along the 2000 km Salinity Gradient of the Baltic Sea2016In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 7, article id 679Article in journal (Refereed)
    Abstract [en]

    Microbial plankton form the productive base of both marine and freshwater ecosystems and are key drivers of global biogeochemical cycles of carbon and nutrients. Plankton diversity is immense with representations from all major phyla within the three domains of life. So far, plankton monitoring has mainly been based on microscopic identification, which has limited sensitivity and reproducibility, not least because of the numerical majority of plankton being unidentifiable under the light microscope. High-throughput sequencing of taxonomic marker genes offers a means to identify taxa inaccessible by traditional methods; thus, recent studies have unveiled an extensive previously unknown diversity of plankton. Here, we conducted ultra-deep Illumina sequencing (average 105 sequences/sample) of rRNA gene amplicons of surface water eukaryotic and bacterial plankton communities sampled in summer along a 2000 km transect following the salinity gradient of the Baltic Sea. Community composition was strongly correlated with salinity for both bacterial and eukaryotic plankton assemblages, highlighting the importance of salinity for structuring the biodiversity within this ecosystem. In contrast, no clear trends in alpha-diversity for bacterial or eukaryotic communities could be detected along the transect. The distribution of major planktonic taxa followed expected patterns as observed in monitoring programs, but groups novel to the Baltic Sea were also identified, such as relatives to the coccolithophore Erniliana huxleyi detected in the northern Baltic Sea. This study provides the first ultra-deep sequencing-based survey on eukaryotic and bacterial plankton biogeography in the Baltic Sea.

  • 4.
    Hu, Yue O. O.
    et al.
    KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Ndegwa, Nelson
    Karolinska Inst, Dept Med Epidemiol & Biostat, Stockholm, Sweden..
    Alneberg, Johannes
    KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Johansson, Sebastian
    Stockholm Univ, Dept Biochem & Biophys, Sci Life Lab, Stockholm, Sweden..
    Logue, Jurg Brendan
    Huss, Mikael
    Käller, Max
    KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Lundeberg, Joakim
    KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Fagerberg, Jens
    Stockholm Vatten Och Avfall AB, Stockholm, Sweden..
    Andersson, Anders F.
    KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Stationary and portable sequencing-based approaches for tracing wastewater contamination in urban stormwater systems2018In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 11907Article in journal (Refereed)
    Abstract [en]

    Urban sewer systems consist of wastewater and stormwater sewers, of which only wastewater is processed before being discharged. Occasionally, misconnections or damages in the network occur, resulting in untreated wastewater entering natural water bodies via the stormwater system. Cultivation of faecal indicator bacteria (e.g. Escherichia coli; E. coli) is the current standard for tracing wastewater contamination. This method is cheap but has limited specificity and mobility. Here, we compared the E. coli culturing approach with two sequencing-based methodologies (Illumina MiSeq 16S rRNA gene amplicon sequencing and Oxford Nanopore MinION shotgun metagenomic sequencing), analysing 73 stormwater samples collected in Stockholm. High correlations were obtained between E. coli culturing counts and frequencies of human gut microbiome amplicon sequences, indicating E. coli is indeed a good indicator of faecal contamination. However, the amplicon data further holds information on contamination source or alternatively how much time has elapsed since the faecal matter has entered the system. Shotgun metagenomic sequencing on a subset of the samples using a portable real-time sequencer, MinION, correlated well with the amplicon sequencing data. This study demonstrates the use of DNA sequencing to detect human faecal contamination in stormwater systems and the potential of tracing faecal contamination directly in the field.

  • 5.
    Hugerth, Luisa W.
    et al.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Muller, Emilie E. L.
    Hu, Yue O. O.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Lebrun, Laura A. M.
    Roume, Hugo
    Lundin, Daniel
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Wilmes, Paul
    Andersson, Anders F.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Systematic Design of 18S rRNA Gene Primers for Determining Eukaryotic Diversity in Microbial Consortia2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 4, p. 095567-Article in journal (Refereed)
    Abstract [en]

    High-throughput sequencing of ribosomal RNA gene (rDNA) amplicons has opened up the door to large-scale comparative studies of microbial community structures. The short reads currently produced by massively parallel sequencing technologies make the choice of sequencing region crucial for accurate phylogenetic assignments. While for 16S rDNA, relevant regions have been well described, no truly systematic design of 18S rDNA primers aimed at resolving eukaryotic diversity has yet been reported. Here we used 31,862 18S rDNA sequences to design a set of broad-taxonomic range degenerate PCR primers. We simulated the phylogenetic information that each candidate primer pair would retrieve using paired-or single-end reads of various lengths, representing different sequencing technologies. Primer pairs targeting the V4 region performed best, allowing discrimination with paired-end reads as short as 150 bp (with 75% accuracy at genus level). The conditions for PCR amplification were optimised for one of these primer pairs and this was used to amplify 18S rDNA sequences from isolates as well as from a range of environmental samples which were then Illumina sequenced and analysed, revealing good concordance between expected and observed results. In summary, the reported primer sets will allow minimally biased assessment of eukaryotic diversity in different microbial ecosystems.

  • 6. Lamei, Sepideh
    et al.
    Hu, Yue O. O.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Olofsson, Tobias C.
    Andersson, Anders F.
    KTH, Centres, Science for Life Laboratory, SciLifeLab. KTH, School of Biotechnology (BIO), Gene Technology.
    Forsgren, Eva
    Vasquez, Alejandra
    Improvement of identification methods for honeybee specific Lactic Acid Bacteria; future approaches2017In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 12, no 3, article id e0174614Article in journal (Refereed)
    Abstract [en]

    Honeybees face many parasites and pathogens and consequently rely on a diverse set of individual and group-level defenses to prevent disease. The crop microbiota of Apis mellifera, composed of 13 Lactic Acid Bacterial (LAB) species within the genera Lactobacillus and Bifidobacterium, form a beneficial symbiotic relationship with each other and the honeybee to protect their niche and their host. Possibly playing a vital role in honeybee health, it is important that these honeybee specific Lactic Acid Bacterial (hbs-LAB) symbionts can be correctly identified, isolated and cultured, to further investigate their health promoting properties. We have previously reported successful identification to the strain level by culture-dependent methods and we recently sequenced and annotated the genomes of the 13 hbs-LAB. However, the hitherto applied techniques are unfortunately very time consuming, expensive and not ideal when analyzing a vast quantity of samples. In addition, other researchers have constantly failed to identify the 13 hbs-LAB from honeybee samples by using inadequate media and/or molecular techniques based on 16S rRNA gene sequencing with insufficient discriminatory power. The aim of this study was to develop better and more suitable methods for the identification and cultivation of hbs-LAB. We compared currently used bacterial cultivation media and could for the first time demonstrate a significant variation in the hbs-LAB basic requirements for optimal growth. We also present a new bacterial identification approach based on amplicon sequencing of a region of the 16S rRNA gene using the Illumina platform and an error correction software that can be used to successfully differentiate and rapidly identify the 13 hbs-LAB to the strain level.

  • 7. Lindh, Markus V.
    et al.
    Sjostedt, Johanna
    Ekstam, Borje
    Casini, Michele
    Lundin, Daniel
    Hugerth, Luisa W.
    KTH, Centres, Science for Life Laboratory, SciLifeLab. KTH, School of Biotechnology (BIO).
    Hu, Yue O. O.
    KTH, School of Biotechnology (BIO). KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Andersson, Anders F.
    KTH, School of Biotechnology (BIO). KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Andersson, Agneta
    Legrand, Catherine
    Pinhassi, Jarone
    Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers2017In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 19, no 3, p. 1222-1236Article in journal (Refereed)
    Abstract [en]

    Metapopulation theory developed in terrestrial ecology provides applicable frameworks for interpreting the role of local and regional processes in shaping species distribution patterns. Yet, empirical testing of metapopulation models on microbial communities is essentially lacking. We determined regional bacterioplankton dynamics from monthly transect sampling in the Baltic Sea Proper using 16S rRNA gene sequencing. A strong positive trend was found between local relative abundance and occupancy of populations. Notably, the occupancy-frequency distributions were significantly bimodal with a satellite mode of rare endemic populations and a core mode of abundant cosmopolitan populations (e.g. Synechococcus, SAR11 and SAR86 clade members). Temporal changes in population distributions supported several theoretical frameworks. Still, bimodality was found among bacterioplankton communities across the entire Baltic Sea, and was also frequent in globally distributed datasets. Datasets spanning waters with widely different physicochemical characteristics or environmental gradients typically lacked significant bimodal patterns. When such datasets were divided into subsets with coherent environmental conditions, bimodal patterns emerged, highlighting the importance of positive feedbacks between local abundance and occupancy within specific biomes. Thus, metapopulation theory applied to microbial biogeography can provide novel insights into the mechanisms governing shifts in biodiversity resulting from natural or anthropogenically induced changes in the environment.

  • 8.
    Lundmark, Anna
    et al.
    Karolinska Inst, Dept Dent Med, Div Periodontol, Huddinge, Sweden..
    Hu, Yue O. O.
    KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab. Karolinska Inst, CTMR, Dept Microbiol Tumor & Cell Biol, Stockholm, Sweden..
    Huss, Mikael
    Stockholm Univ, Natl Bioinformat Infrastruct Sweden, Dept Biochem & Biophys, Sci Life Lab, Solna, Sweden..
    Johannsen, Gunnar
    Karolinska Inst, Dept Dent Med, Div Periodontol, Huddinge, Sweden..
    Andersson, Anders F.
    KTH, School of Engineering Sciences in Chemistry, Biotechnology and Health (CBH), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Yucel-Lindberg, Tulay
    Karolinska Inst, Dept Dent Med, Div Periodontol, Huddinge, Sweden..
    Identification of Salivary Microbiota and Its Association With Host Inflammatory Mediators in Periodontitis2019In: Frontiers in Cellular and Infection Microbiology, E-ISSN 2235-2988, Vol. 9, article id 216Article in journal (Refereed)
    Abstract [en]

    Periodontitis is a microbial-induced chronic inflammatory disease, which may not only result in tooth loss, but can also contribute to the development of various systemic diseases. The transition from healthy to diseased periodontium depends on microbial dysbiosis and impaired host immune response. Although periodontitis is a common disease as well as associated with various systemic inflammatory conditions, the taxonomic profiling of the salivary microbiota in periodontitis and its association with host immune and inflammatory mediators has not been reported. Therefore, the aim of this study was to identify key pathogens and their potential interaction with the host's inflammatory mediators in saliva samples for periodontitis risk assessment. The microbial 16S rRNA gene sequencing and the levels of inflammatory mediators were performed in saliva samples from patients with chronic periodontitis and periodontally healthy control subjects. The salivary microbial community composition differed significantly between patients with chronic periodontitis and healthy controls. Our analyses identified a number of microbes, including bacteria assigned to Eubacterium saphenum, Tannerella forsythia, Filifactor alocis, Streptococcus mitis/parasanguinis, Parvimonas micra, Prevotella sp., Phocaeicola sp., and Fretibacterium sp. as more abundant in periodontitis, compared to healthy controls. In samples from healthy individuals, we identified Campylobacter concisus, and Veillonella sp. as more abundant. Integrative analysis of the microbiota and inflammatory mediators/cytokines revealed associations that included positive correlations between the pathogens Treponema sp. and Selenomas sp. and the cytokines chitinase 3-like 1, sIL-6R alpha, sTNF-R1, and gp 130/sIL-6R beta. In addition, a negative correlation was identified between IL-10 and Filifactor alocis. Our results reveal distinct and disease-specific patterns of salivary microbial composition between patients with periodontitis and healthy controls, as well as significant correlations between microbiota and host-mediated inflammatory cytokines. The positive correlations between the pathogens Treponema sp. and Selenomas sp. and the cytokines chitinase 3-like 1, sIL-6R alpha, sTNF-R1, and gp 130/sIL-6R beta might have the future potential to serve as a combined bacteria-host salivary biomarker panel for diagnosis of the chronic infectious disease periodontitis. However, further studies are required to determine the capacity of these microbes and inflammatory mediators as a salivary biomarker panel for periodontitis.

  • 9.
    Thureborn, Petter
    et al.
    Södertörn University, School of Natural Sciences, Technology and Environmental Studies, Environmental Science..
    Hu, Yue
    KTH, School of Biotechnology (BIO).
    Franzetti, Andrea
    University of Milano-Bicocca, Milano, Italy..
    Sjöling, Sara
    Södertörn University, School of Natural Sciences, Technology and Environmental Studies, Environmental Science..
    Lundin, Daniel
    Linnaeus University, Department of Biology and Environmental Science..
    Accumulation of DNA in an anoxic sediment – rDNA and rRNA presence of members of the microbial community from Landsort Deep, the Baltic SeaManuscript (preprint) (Other academic)
    Abstract [en]

    Numerous investigations of bacterial communities using sequence analysis of environmental DNA have revealed extensive diversity of microbial taxa in an array of different environmental habitats. Community analysis based solely on DNA, however, does not reveal whether the detected community members are actively contributing to community functioning, or whether they are dormant or remnants of dead cells. This dilemma is of particular concern when analyzing microbial community structure of sites with a high degree of deposited matter, such as marine sediments. For example, the Baltic Sea’s deepest point, the Landsort Deep, consists of anoxic sediments with a large deposition of allochthonous organic matter from the highly stratified 460 m water column above. Our previous metagenomics results indicated the presence of potential obligately aerobic and phototrophic microorganisms in the Landsort Deep sediment. To further elucidate which taxa may contribute to ecosystem function at this site, we here present three different datasets – rDNA amplicons, rDNA reads from a shotgun metagenome and expressed rRNA from a shotgun metatranscriptome. By comparing the three datasets and the ratios between rRNA and rDNA we seek to estimate the protein synthesis potential of the community members in order to provide an indication of what taxa may have cellular activity and metabolic potential. The variation in protein synthesis potential was large, both within and between taxa, in the sediment community. Many typically anaerobic taxa, e.g. from Deltaproteobacteria and Euryarchaeota, showed a high protein synthesis potential, while typical aerobes like Flavobacteria showed a low protein synthesis potential. More surprisingly, some common Baltic Sea surface water bacteria also displayed a high protein synthesis potential, suggesting they have an active role in the anoxic sediment ecosystem at 460 m depth. Both filamentous and unicellular Cyanobacteria exhibited very high protein synthesis potential, which implies a more complex role of these bacteria in carbon cycling in the Baltic Sea than previously suggested. Moreover, Mycobacteria, that were abundant in Landsort Deep sediment metagenome compared with other marine sediment metagenomes, showed protein synthesis potentials consistent with a functional role in the sediment community. Our results provide a new window of insight into the complexities of the microbial community of Landsort Deep with implications for the understanding of other anoxic accumulation sediments.

  • 10. Zhu, X.
    et al.
    Shen, Y.
    Chen, X.
    Hu, Yue O. O.
    KTH, School of Biotechnology (BIO), Gene Technology. KTH, Centres, Science for Life Laboratory, SciLifeLab.
    Xiang, H.
    Tao, J.
    Ling, Y.
    Biodegradation mechanism of microcystin-LR by a novel isolate of Rhizobium sp. TH and the evolutionary origin of the mlrA gene2016In: International Biodeterioration & Biodegradation, ISSN 0964-8305, E-ISSN 1879-0208, Vol. 115, p. 17-25Article in journal (Refereed)
    Abstract [en]

    The frequent presence of microcystin (MC) in eutrophic water bodies worldwide poses a serious threat to ecosystems. Biodegradation has been extensively investigated as a main pathway for MC attenuation, and an mlr-dependent mechanism of MC degradation have been elucidated in detail. However, the evolutionary origin and the distribution of mlr genes in MC-degrading bacteria is poorly understood. In this study, a novel Rhizobium sp. TH, which is the first α-proteobacterial MC-degrading bacterium other than Sphingomonadales, was isolated. Strain TH degraded MC via the mlr-dependent mechanism with a first-order rate constant of 0.18–0.29 h−1 under near-natural conditions. The partial length mlr gene cluster was sequenced, and the function of its key gene, mlrA, was verified by heterologous expression in Escherichia coli. Phylogenetic analyses show that the mlrA gene initially arose in α-proteobacteria by vertical evolution, and the two strains from β- and γ-proteobacteria acquired it by horizontal gene transfer. Therefore, the mlrA gene mainly exists in α-proteobacteria but is seldom present in other bacteria. A pair of primers matching well with mlrA sequences reported so far were designed and could be used to determine the MC-degrading mechanism for novel isolates or to screen for MC-degrading ability among environmental samples.

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