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Bunse, C., Israelsson, S., Baltar, F., Bertos-Fortis, M., Fridolfsson, E., Legrand, C., . . . Pinhassi, J. (2019). High Frequency Multi-Year Variability in Baltic Sea Microbial Plankton Stocks and Activities. Frontiers in Microbiology, 9, Article ID 3296.
Open this publication in new window or tab >>High Frequency Multi-Year Variability in Baltic Sea Microbial Plankton Stocks and Activities
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2019 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 9, article id 3296Article in journal (Refereed) Published
Abstract [en]

Marine bacterioplankton are essential in global nutrient cycling and organic matter turnover. Time-series analyses, often at monthly sampling frequencies, have established the paramount role of abiotic and biotic variables in structuring bacterioplankton communities and productivities. However, fine-scale seasonal microbial activities, and underlying biological principles, are not fully understood. We report results from four consecutive years of high-frequency time-series sampling in the Baltic Proper. Pronounced temporal dynamics in most investigated microbial variables were observed, including bacterial heterotrophic production, plankton biomass, extracellular enzyme activities, substrate uptake rate constants of glucose, pyruvate, acetate, amino acids, and leucine, as well as nutrient limitation bioassays. Spring blooms consisting of diatoms and dinoflagellates were followed by elevated bacterial heterotrophic production and abundances. During summer, bacterial productivity estimates increased even further, coinciding with an initial cyanobacterial bloom in early July. However, bacterial abundances only increased following a second cyanobacterial bloom, peaking in August. Uptake rate constants for the different measured carbon compounds varied seasonally and inter-annually and were highly correlated to bacterial productivity estimates, temperature, and cyanobacterial abundances. Further, we detected nutrient limitation in response to environmental conditions in a multitude of microbial variables, such as elevated productivities in nutrient bioassays, changes in enzymatic activities, or substrate preferences. Variations among biotic variables often occurred on time scales of days to a few weeks, yet often spanning several sampling occasions. Such dynamics might not have been captured by sampling at monthly intervals, as compared to more predictable transitions in abiotic variables such as temperature or nutrient concentrations. Our study indicates that high resolution analyses of microbial biomass and productivity parameters can help out in the development of biogeochemical and food web models disentangling the microbial black box.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2019
Keywords
marine bacteria, phytoplankton, cyanobacteria, production, substrate uptake, enzyme activity, biogeochemistry
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-80150 (URN)10.3389/fmicb.2018.03296 (DOI)000455948100001 ()
Available from: 2019-02-05 Created: 2019-02-05 Last updated: 2019-02-05Bibliographically approved
Zhang, H., Yoshizawa, S., Sun, Y., Huang, Y., Chu, X., Gonzalez, J. M., . . . Luo, H. (2019). Repeated evolutionary transitions of flavobacteria from marine to non-marine habitats. Environmental Microbiology, 21(2), 648-666
Open this publication in new window or tab >>Repeated evolutionary transitions of flavobacteria from marine to non-marine habitats
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2019 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 21, no 2, p. 648-666Article in journal (Refereed) Published
Abstract [en]

The taxonomy of marine and non-marine organisms rarely overlap, but the mechanisms underlying this distinction are often unknown. Here, we predicted three major ocean-to-land transitions in the evolutionary history of Flavobacteriaceae, a family known for polysaccharide and peptide degradation. These unidirectional transitions were associated with repeated losses of marine signature genes and repeated gains of non-marine adaptive genes. This included various Na+-dependent transporters, osmolyte transporters and glycoside hydrolases (GH) for sulfated polysaccharide utilization in marine descendants, and in non-marine descendants genes for utilizing the land plant material pectin and genes facilitating terrestrial host interactions. The K+ scavenging ATPase was repeatedly gained whereas the corresponding low-affinity transporter repeatedly lost upon transitions, reflecting K+ ions are less available to non-marine bacteria. Strikingly, the central metabolism Na+-translocating NADH: quinone dehydrogenase gene was repeatedly gained in marine descendants, whereas the H+-translocating counterpart was repeatedly gained in non-marine lineages. Furthermore, GH genes were depleted in isolates colonizing animal hosts but abundant in bacteria inhabiting other non-marine niches; thus relative abundances of GH versus peptidase genes among Flavobacteriaceae lineages were inconsistent with the marine versus non-marine dichotomy. We suggest that phylogenomic analyses can cast novel light on mechanisms explaining the distribution and ecology of key microbiome components.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2019
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-81225 (URN)10.1111/1462-2920.14509 (DOI)000459172700011 ()30565818 (PubMedID)
Available from: 2019-03-22 Created: 2019-03-22 Last updated: 2019-03-22Bibliographically approved
Alneberg, J., Sundh, J., Bennke, C., Beier, S., Lundin, D., Hugerth, L. W., . . . Andersson, A. F. (2018). BARM and BalticMicrobeDB, a reference metagenome and interface to meta-omic data for the Baltic Sea. Scientific Data, 5, Article ID 180146.
Open this publication in new window or tab >>BARM and BalticMicrobeDB, a reference metagenome and interface to meta-omic data for the Baltic Sea
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2018 (English)In: Scientific Data, E-ISSN 2052-4463, Vol. 5, article id 180146Article in journal (Refereed) Published
Abstract [en]

The Baltic Sea is one of the world's largest brackish water bodies and is characterised by pronounced physicochemical gradients where microbes are the main biogeochemical catalysts. Meta-omic methods provide rich information on the composition of, and activities within, microbial ecosystems, but are computationally heavy to perform. We here present the Baltic Sea Reference Metagenome (BARM), complete with annotated genes to facilitate further studies with much less computational effort. The assembly is constructed using 2.6 billion metagenomic reads from 81 water samples, spanning both spatial and temporal dimensions, and contains 6.8 million genes that have been annotated for function and taxonomy. The assembly is useful as a reference, facilitating taxonomic and functional annotation of additional samples by simply mapping their reads against the assembly. This capability is demonstrated by the successful mapping and annotation of 24 external samples. In addition, we present a public web interface, BalticMicrobeDB, for interactive exploratory analysis of the dataset. [GRAPHICS] .

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Bioinformatics and Systems Biology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-77392 (URN)10.1038/sdata.2018.146 (DOI)000440291200001 ()30063227 (PubMedID)
Available from: 2018-08-29 Created: 2018-08-29 Last updated: 2018-10-24Bibliographically approved
Alneberg, J., Karlsson, C. M. G., Divne, A.-M., Bergin, C., Homa, F., Lindh, M. V., . . . Pinhassi, J. (2018). Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes. Microbiome, 6, Article ID 173.
Open this publication in new window or tab >>Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes
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2018 (English)In: Microbiome, ISSN 0026-2633, E-ISSN 2049-2618, Vol. 6, article id 173Article in journal (Refereed) Published
Abstract [en]

Background: Prokaryotes dominate the biosphere and regulate biogeochemical processes essential to all life. Yet, our knowledge about their biology is for the most part limited to the minority that has been successfully cultured. Molecular techniques now allow for obtaining genome sequences of uncultivated prokaryotic taxa, facilitating in-depth analyses that may ultimately improve our understanding of these key organisms. Results: We compared results from two culture-independent strategies for recovering bacterial genomes: single-amplified genomes and metagenome-assembled genomes. Single-amplified genomes were obtained from samples collected at an offshore station in the Baltic Sea Proper and compared to previously obtained metagenome-assembled genomes from a time series at the same station. Among 16 single-amplified genomes analyzed, seven were found to match metagenome-assembled genomes, affiliated with a diverse set of taxa. Notably, genome pairs between the two approaches were nearly identical (average 99.51% sequence identity; range 98.77-99.84%) across overlapping regions (30-80% of each genome). Within matching pairs, the single-amplified genomes were consistently smaller and less complete, whereas the genetic functional profiles were maintained. For the metagenome-assembled genomes, only on average 3.6% of the bases were estimated to be missing from the genomes due to wrongly binned contigs. Conclusions: The strong agreement between the single-amplified and metagenome-assembled genomes emphasizes that both methods generate accurate genome information from uncultivated bacteria. Importantly, this implies that the research questions and the available resources are allowed to determine the selection of genomics approach for microbiome studies.

Place, publisher, year, edition, pages
BioMed Central, 2018
Keywords
Single-amplified genomes, Metagenome-assembled genomes, Metagenomics, Binning, Single-cell genomics
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-78465 (URN)10.1186/s40168-018-0550-0 (DOI)000446307400001 ()30266101 (PubMedID)
Available from: 2018-10-24 Created: 2018-10-24 Last updated: 2018-10-24Bibliographically approved
Paerl, R. W., Sundh, J., Tan, D., Svenningsen, S. L., Hylander, S., Pinhassi, J., . . . Riemann, L. (2018). Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability. Proceedings of the National Academy of Sciences of the United States of America, 115(44), E10447-E10456
Open this publication in new window or tab >>Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability
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2018 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 44, p. E10447-E10456Article in journal (Refereed) Published
Abstract [en]

Vitamin B1 (B1 herein) is a vital enzyme cofactor required by virtually all cells, including bacterioplankton, which strongly influence aquatic biogeochemistry and productivity and modulate climate on Earth. Intriguingly, bacterioplankton can be de novo B1 synthesizers or B1 auxotrophs, which cannot synthesize B1 de novo and require exogenous B1 or B1 precursors to survive. Recent isolate-based work suggests select abundant bacterioplankton are B1 auxotrophs, but direct evidence of B1 auxotrophy among natural communities is scant. In addition, it is entirely unknown if bulk bacterioplankton growth is ever B1-limited. We show by surveying for B1-related genes in estuarine, marine, and freshwater metagenomes and metagenome-assembled genomes (MAGs) that most naturally occurring bacterioplankton are B1 auxotrophs. Pyrimidine B1-auxotrophic bacterioplankton numerically dominated metagenomes, but multiple other B1-auxotrophic types and distinct uptake and B1-salvaging strategies were also identified, including dual (pyrimidine and thiazole) and intact B1 auxotrophs that have received little prior consideration. Time-series metagenomes from the Baltic Sea revealed pronounced shifts in the prevalence of multiple B1-auxotrophic types and in the B1-uptake and B1-salvaging strategies over time. Complementarily, we documented B1/precursor limitation of bacterioplankton production in three of five nutrient-amendment experiments at the same time-series station, specifically when intact B1 concentrations were ≤3.7 pM, based on bioassays with a genetically engineered Vibrio anguillarum B1-auxotrophic strain. Collectively, the data presented highlight the prevalent reliance of bacterioplankton on exogenous B1/precursors and on the bioavailability of the micronutrients as an overlooked factor that could influence bacterioplankton growth and succession and thereby the cycling of nutrients and energy in aquatic systems.

Place, publisher, year, edition, pages
National Academy of Sciences, 2018
Keywords
vitamin B1, thiamin, bacterioplankton, metagenomics, growth limitation
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-78320 (URN)10.1073/pnas.1806425115 (DOI)000448713200018 ()30322929 (PubMedID)
Available from: 2018-10-16 Created: 2018-10-16 Last updated: 2018-11-15Bibliographically approved
Berner, C., Bertos-Fortis, M., Pinhassi, J. & Legrand, C. (2018). Response of Microbial Communities to Changing Climate Conditions During Summer Cyanobacterial Blooms in the Baltic Sea. Frontiers in Microbiology, 9, Article ID 1562.
Open this publication in new window or tab >>Response of Microbial Communities to Changing Climate Conditions During Summer Cyanobacterial Blooms in the Baltic Sea
2018 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 9, article id 1562Article in journal (Refereed) Published
Abstract [en]

Frequencies and biomass of Baltic Sea cyanobacterial blooms are expected to be higher in future climate conditions, but also of longer duration as a result of increased sea surface temperature. Concurrently, climate predictions indicate a reduced salinity in the Baltic Sea. These climate-driven changes are expected to alter not solely the phytoplankton community but also the role of microbial communities for nutrient remineralization. Here, we present the response of summer plankton communities (filamentous cyanobacteria, picocyanobacteria, and heterotrophic bacteria) to the interplay of increasing temperature (from 16 to 18 degrees C and 20 degrees C) and reduced salinity (from salinity 6.9 to 5.9) in the Baltic Proper (NW Gotland Sea) using a microcosm approach. Warmer temperatures led to an earlier peak of cyanobacterial biomass, while yields were reduced. These conditions caused a decrease of nitrogen-fixers (Dolichospermum sp.) biomass, while non nitrogen-fixers (Pseudanabaena sp.) increased. Salinity reduction did not affect cyanobacterial growth nor community composition. Among heterotrophic bacteria, Actinobacteria showed preference for high temperature, while Gammaproteobacteria thrived at in situ temperature. Heterotrophic bacteria community changed drastically at lower salinity and resembled communities at high temperature. Picocyanobacteria and heterotrophic bacterial biomass had a pronounced increase associated with the decay of filamentous cyanobacteria. This suggests that shifts in community composition of heterotrophic bacteria are influenced both directly by abiotic factors (temperature and salinity) and potentially indirectly by cyanobacteria. Our findings suggest that at warmer temperature, lower yield of photosynthetic cyanobacteria combined with lower proportion of nitrogen-fixers in the community could result in lower carbon export to the marine food web with consequences for the decomposer community of heterotrophic bacteria.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
Keywords
microscopy, 16S rRNA, cyanobacteria, heterotrophic bacteria, biomass, summer bloom, Baltic Sea, climate change
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-77393 (URN)10.3389/fmicb.2018.01562 (DOI)000439753100001 ()30090087 (PubMedID)
Available from: 2018-08-29 Created: 2018-08-29 Last updated: 2018-08-29Bibliographically approved
Lindh, M. V. & Pinhassi, J. (2018). Sensitivity of Bacterioplankton to Environmental Disturbance: A Review of Baltic Sea Field Studies and Experiments. Frontiers in Marine Science, 5, 1-17, Article ID UNSP 361.
Open this publication in new window or tab >>Sensitivity of Bacterioplankton to Environmental Disturbance: A Review of Baltic Sea Field Studies and Experiments
2018 (English)In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 5, p. 1-17, article id UNSP 361Article, review/survey (Refereed) Published
Abstract [en]

Bacterioplankton communities regulate energy and matter fluxes fundamental to all aquatic life. The Baltic Sea offers an outstanding ecosystem for interpreting causes and consequences of bacterioplankton community composition shifts resulting from environmental disturbance. Yet, a systematic synthesis of the composition of Baltic Sea bacterioplankton and their responses to natural or human-induced environmental perturbations is lacking. We review current research on Baltic Sea bacterioplankton dynamics in situ (48 articles) and in laboratory experiments (38 articles) carried out at a variety of spatiotemporal scales. In situ studies indicate that the salinity gradient sets the boundaries for bacterioplankton composition, whereas, regional environmental conditions at a within-basin scale, including the level of hypoxia and phytoplankton succession stages, may significantly tune the composition of bacterial communities. Also the experiments show that Baltic Sea bacteria are highly responsive to environmental conditions, with general influences of e.g. salinity, temperature and nutrients. Importantly, nine out of ten experiments that measured both bacterial community composition and some metabolic activities showed empirical support for the sensitivity scenario of bacteria - i.e., that environmental disturbance caused concomitant change in both community composition and community functioning. The lack of studies empirically testing the resilience scenario, i.e., experimental studies that incorporate the long-term temporal dimension, precludes conclusions about the potential prevalence of resilience of Baltic Sea bacterioplankton. We also outline outstanding questions emphasizing promising applications in incorporating bacterioplankton community dynamics into biogeochemical and food-web models and the lack of knowledge for deep-sea assemblages, particularly bacterioplankton structure-function relationships. This review emphasizes that bacterioplankton communities rapidly respond to natural and predicted human-induced environmental disturbance by altering their composition and metabolic activity. Unless bacterioplankton are resilient, such changes could have severe consequences for the regulation of microbial ecosystem services.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
Keywords
bacterial diversity, archaea, 16S rRNA, metabolic activity, ecosystem functioning, climate change
National Category
Ecology Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-80567 (URN)10.3389/fmars.2018.00361 (DOI)000457522700001 ()
Available from: 2019-02-19 Created: 2019-02-19 Last updated: 2019-02-19Bibliographically approved
Muthusamy, S. D., Lundin, D., Branca, R. M., Baltar, F., Gonzalez, J. M., Lehtio, J. & Pinhassi, J. (2017). Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria. Environmental Microbiology, 19(6), 2301-2319
Open this publication in new window or tab >>Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria
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2017 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 19, no 6, p. 2301-2319Article, review/survey (Refereed) Published
Abstract [en]

Much of the phenotype of a microorganism consists of its repertoire of metabolisms and how and when its proteins are deployed under different growth conditions. Hence, analyses of protein expression could provide important understanding of how bacteria adapt to different environmental settings. To characterize the flexibility of proteomes of marine bacteria, we investigated protein profiles of three important marine bacterial lineages - Oceanospirillaceae (Neptuniibacter caesariensis strain MED92), Roseobacter (Phaeobacter sp. MED193) and Flavobacteria (Dokdonia sp. MED134) - during transition from exponential to stationary phase. As much as 59-80% of each species' total proteome was expressed. Moreover, all three bacteria profoundly altered their expressed proteomes during growth phase transition, from a dominance of proteins involved in translation to more diverse proteomes, with a striking appearance of enzymes involved in different nutrient-scavenging metabolisms. Whereas the three bacteria shared several overarching metabolic strategies, they differed in important details, including distinct expression patterns of membrane transporters and proteins in carbon and phosphorous metabolism and storage compounds. These differences can be seen as signature metabolisms - metabolisms specific for lineages. These findings suggest that quantitative proteomics can inform about the divergent ecological strategies of marine bacteria in adapting to changes in environmental conditions.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2017
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-66909 (URN)10.1111/1462-2920.13725 (DOI)000404007700018 ()
Available from: 2017-07-13 Created: 2017-07-13 Last updated: 2018-02-06Bibliographically approved
Bunse, C. & Pinhassi, J. (2017). Marine bacterioplankton seasonal succession dynamics. Trends in Microbiology, 25(6), 495-505
Open this publication in new window or tab >>Marine bacterioplankton seasonal succession dynamics
2017 (English)In: Trends in Microbiology, ISSN 0966-842X, E-ISSN 1878-4380, Vol. 25, no 6, p. 495-505Article in journal (Refereed) Published
Abstract [en]

Bacterioplankton (bacteria and archaea) are indispensable regulators of global element cycles owing to their unique ability to decompose and remineralize dissolved organic matter. These microorganisms in surface waters worldwide exhibit pronounced seasonal succession patterns, governed by physicochemical factors (e.g., light, climate, and nutrient loading) that are determined by latitude and distance to shore. Moreover, we emphasize that the effects of large-scale factors are modulated regionally, and over shorter timespans (days to weeks), by biological interactions including molecule exchanges, viral lysis, and grazing. Thus the interplay and scaling between factors ultimately determine the success of particular bacterial populations. Spatiotemporal surveys of bacterioplankton community composition provide the necessary frame for interpreting how the distinct metabolisms encoded in the genomes of different bacteria regulate biogeochemical cycles.

Place, publisher, year, edition, pages
Elsevier, 2017
National Category
Biological Sciences
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-60291 (URN)10.1016/j.tim.2016.12.013 (DOI)000401231800011 ()28108182 (PubMedID)
Projects
EcoChange
Available from: 2017-01-27 Created: 2017-01-27 Last updated: 2018-10-24Bibliographically approved
Lindh, M. V., Sjöstedt, J., Ekstam, B., Casini, M., Lundin, D., Hugerth, L., . . . Pinhassi, J. (2017). Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers. Environmental Microbiology, 19(3), 1222-1236
Open this publication in new window or tab >>Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers
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2017 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 19, no 3, p. 1222-1236Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2017
National Category
Ecology Microbiology
Research subject
Ecology, Microbiology; Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-61540 (URN)10.1111/1462-2920.13650 (DOI)000397525100031 ()28028880 (PubMedID)
Projects
EcoChange
Available from: 2017-03-21 Created: 2017-03-21 Last updated: 2019-02-27Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-6405-1347

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