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Delgadillo-Nuno, E., Teira, E., Pontiller, B., Lundin, D., Joglar, V., Pedros-Alio, C., . . . Martinez-Garcia, S. (2024). Coastal upwelling systems as dynamic mosaics of bacterioplankton functional specialization. Frontiers in Marine Science, 10, Article ID 1259783.
Open this publication in new window or tab >>Coastal upwelling systems as dynamic mosaics of bacterioplankton functional specialization
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2024 (English)In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 10, article id 1259783Article in journal (Refereed) Published
Abstract [en]

Coastal upwelling areas are extraordinarily productive environments where prokaryotic communities, the principal remineralizers of dissolved organic matter (DOM), rapidly respond to phytoplankton bloom and decay dynamics. Nevertheless, the extent of variability of key microbial functions in such dynamic waters remains largely unconstrained. Our metatranscriptomics analyses of 162 marker genes encoding ecologically relevant prokaryotic functions showed distinct spatial-temporal patterns in the NW Iberian Peninsula upwelling area. Short-term (daily) changes in specific bacterial functions associated with changes in biotic and abiotic factors were superimposed on seasonal variability. Taxonomic and functional specialization of prokaryotic communities, based mostly on different resource acquisition strategies, was observed. Our results uncovered the potential influence of prokaryotic functioning on phytoplankton bloom composition and development (e.g., Cellvibrionales and Flavobacteriales increased relative gene expression related to vitamin B12 and siderophore metabolisms during Chaetoceros and Dinophyceae summer blooms). Notably, bacterial adjustments to C- or N-limitation and DMSP availability during summer phytoplankton blooms and different spatial-temporal patterns of variability in the expression of genes with different phosphate affinity indicated a complex role of resource availability in structuring bacterial communities in this upwelling system. Also, a crucial role of Cellvibrionales in the degradation of DOM (carbohydrate metabolism, TCA cycle, proteorhodopsin, ammonium, and phosphate uptake genes) during the summer phytoplankton bloom was found. Overall, this dataset revealed an intertwined mosaic of microbial interactions and nutrient utilization patterns along a spatial-temporal gradient that needs to be considered if we aim to understand the biogeochemical processes in some of the most productive ecosystems in the world ' s oceans.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2024
Keywords
bacterioplankton, upwelling systems, phytoplankton bloom, metatranscriptomics, metabarcoding
National Category
Microbiology Oceanography, Hydrology and Water Resources
Research subject
Ecology, Microbiology; Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-127387 (URN)10.3389/fmars.2023.1259783 (DOI)001143516000001 ()2-s2.0-85182436775 (Scopus ID)
Available from: 2024-02-01 Created: 2024-02-01 Last updated: 2024-03-13Bibliographically approved
Capo, E., Peterson, B. D., Kim, M., Jones, D. S., Acinas, S. G., Amyot, M., . . . Gionfriddo, C. M. (2023). A consensus protocol for the recovery of mercury methylation genes from metagenomes. Molecular Ecology Resources, 23(1), 190-204
Open this publication in new window or tab >>A consensus protocol for the recovery of mercury methylation genes from metagenomes
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2023 (English)In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 23, no 1, p. 190-204Article in journal (Refereed) Published
Abstract [en]

Mercury (Hg) methylation genes (hgcAB) mediate the formation of the toxic methylmercury and have been identified from diverse environments, including freshwater and marine ecosystems, Arctic permafrost, forest and paddy soils, coal-ash amended sediments, chlor-alkali plants discharges and geothermal springs. Here we present the first attempt at a standardized protocol for the detection, identification and quantification of hgc genes from metagenomes. Our Hg-cycling microorganisms in aquatic and terrestrial ecosystems (Hg-MATE) database, a catalogue of hgc genes, provides the most accurate information to date on the taxonomic identity and functional/metabolic attributes of microorganisms responsible for Hg methylation in the environment. Furthermore, we introduce "marky-coco", a ready-to-use bioinformatic pipeline based on de novo single-metagenome assembly, for easy and accurate characterization of hgc genes from environmental samples. We compared the recovery of hgc genes from environmental metagenomes using the marky-coco pipeline with an approach based on coassembly of multiple metagenomes. Our data show similar efficiency in both approaches for most environments except those with high diversity (i.e., paddy soils) for which a coassembly approach was preferred. Finally, we discuss the definition of true hgc genes and methods to normalize hgc gene counts from metagenomes.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
Keywords
bioinformatics, hg methylation, hgcAB genes, hg-MATE, marky-coco, mercury, metagenomics
National Category
Bioinformatics and Systems Biology Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-116300 (URN)10.1111/1755-0998.13687 (DOI)000836019100001 ()35839241 (PubMedID)2-s2.0-85135534585 (Scopus ID)
Available from: 2022-09-16 Created: 2022-09-16 Last updated: 2023-02-17Bibliographically approved
Churakova, Y., Aguilera, A., Charalampous, E., Conley, D. J., Lundin, D., Pinhassi, J. & Farnelid, H. (2023). Biogenic silica accumulation in picoeukaryotes: Novel players in the marine silica cycle. Environmental Microbiology Reports, 15(4), 282-290
Open this publication in new window or tab >>Biogenic silica accumulation in picoeukaryotes: Novel players in the marine silica cycle
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2023 (English)In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 15, no 4, p. 282-290Article in journal (Refereed) Published
Abstract [en]

It is well known that the biological control of oceanic silica cycling is dominated by diatoms, with sponges and radiolarians playing additional roles. Recent studies have revealed that some smaller marine organisms (e.g. the picocyanobacterium Synechococcus) also take up silicic acid (dissolved silica, dSi) and accumulate silica, despite not exhibiting silicon dependent cellular structures. Here, we show biogenic silica (bSi) accumulation in five strains of picoeukaryotes (<2-3 mu m), including three novel isolates from the Baltic Sea, and two marine species (Ostreococcus tauri and Micromonas commoda), in cultures grown with added dSi (100 mu M). Average bSi accumulation in these novel biosilicifiers was between 30 and 92 amol Si cell(-1). Growth rate and cell size of the picoeukaryotes were not affected by dSi addition. Still, the purpose of bSi accumulation in these smaller eukaryotic organisms lacking silicon dependent structures remains unclear. In line with the increasing recognition of picoeukaryotes in biogeochemical cycling, our findings suggest that they can also play a significant role in silica cycling.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-120915 (URN)10.1111/1758-2229.13144 (DOI)000966621000001 ()36992638 (PubMedID)2-s2.0-85152072762 (Scopus ID)
Available from: 2023-05-26 Created: 2023-05-26 Last updated: 2023-09-07Bibliographically approved
Seidel, L., Broman, E., Nilsson, E., Ståhle, M., Ketzer, J. M., Pérez Martínez, C., . . . Dopson, M. (2023). Climate change-related warming reduces thermal sensitivity and modifies metabolic activity of coastal benthic bacterial communities. The ISME Journal, 17, 855-869
Open this publication in new window or tab >>Climate change-related warming reduces thermal sensitivity and modifies metabolic activity of coastal benthic bacterial communities
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2023 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 17, p. 855-869Article in journal (Refereed) Published
Abstract [en]

Besides long-term average temperature increases, climate change is projected to result in a higher frequency of marine heatwaves. Coastal zones are some of the most productive and vulnerable ecosystems, with many stretches already under anthropogenic pressure. Microorganisms in coastal areas are central to marine energy and nutrient cycling and therefore, it is important to understand how climate change will alter these ecosystems. Using a long-term heated bay (warmed for 50 years) in comparison with an unaffected adjacent control bay and an experimental short-term thermal (9 days at 6–35 °C) incubation experiment, this study provides new insights into how coastal benthic water and surface sediment bacterial communities respond to temperature change. Benthic bacterial communities in the two bays reacted differently to temperature increases with productivity in the heated bay having a broader thermal tolerance compared with that in the control bay. Furthermore, the transcriptional analysis showed that the heated bay benthic bacteria had higher transcript numbers related to energy metabolism and stress compared to the control bay, while short-term elevated temperatures in the control bay incubation experiment induced a transcript response resembling that observed in the heated bay field conditions. In contrast, a reciprocal response was not observed for the heated bay community RNA transcripts exposed to lower temperatures indicating a potential tipping point in community response may have been reached. In summary, long-term warming modulates the performance, productivity, and resilience of bacterial communities in response to warming.

Place, publisher, year, edition, pages
Springer Nature, 2023
Keywords
Climate change, bacterial production, RNA-Seq., 16S rRNA gene amplicon sequencing, thermal performance, benthic zone
National Category
Bioinformatics and Systems Biology Microbiology Climate Research Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-111587 (URN)10.1038/s41396-023-01395-z (DOI)000959217900001 ()36977742 (PubMedID)2-s2.0-85151163130 (Scopus ID)
Note

Is included in the dissertation as a manuscript titled: Climate change related warming reduces thermal sensitivity of performance and metabolic plasticity of benthic zone bacterial communities

Available from: 2022-04-25 Created: 2022-04-25 Last updated: 2023-05-25Bibliographically approved
Aguilera, A., Alegria Zufia, J., Bas Conn, L., Gurlit, L., Śliwińska‐Wilczewska, S., Budzałek, G., . . . Farnelid, H. (2023). Ecophysiological analysis reveals distinct environmental preferences in closely related Baltic Sea picocyanobacteria. Environmental Microbiology, 25(9), 1674-1695
Open this publication in new window or tab >>Ecophysiological analysis reveals distinct environmental preferences in closely related Baltic Sea picocyanobacteria
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2023 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 25, no 9, p. 1674-1695Article in journal (Refereed) Published
Abstract [en]

Cluster 5 picocyanobacteria significantly contribute to primary productivity in aquatic ecosystems. Estuarine populations are highly diverse and consist of many co-occurring strains, but their physiology remains largely understudied. In this study, we characterized 17 novel estuarine picocyanobacterial strains. Phylogenetic analysis of the 16S rRNA and pigment genes (cpcBandcpeBA) uncovered multiple estuarine and freshwater-related clusters and pigment types. Assays with five representative strains (three phycocyanin rich and two phycoerythrin rich) under temperature (10–30°C), light(10–190 μmol  photons  m-2s-1), and salinity (2–14  PSU) gradients revealed distinct growth optima and tolerance, indicating that genetic variability was accompanied by physiological diversity. Adaptability to environmental conditions was associated with differential pigment content and photosynthetic performance. Amplicon sequence variants at a coastal and an offshore station linked population dynamics with phylogenetic clusters, supporting that strains isolated in this study represent key ecotypes within the Baltic Sea picocyanobacterial community. The functional diversity found within strains with the same pigment type suggests that understanding estuarine picocyanobacterial ecology requires analysis beyond the phycocyanin and phycoerythrin divide. This new knowledge of the environmental preferences in estuarine picocyanobacteria is important for understanding and evaluating productivity in current and future ecosystems.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
National Category
Environmental Sciences Ecology Microbiology
Research subject
Natural Science, Environmental Science; Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-120317 (URN)10.1111/1462-2920.16384 (DOI)000973717000001 ()2-s2.0-85153326236 (Scopus ID)
Funder
Knut and Alice Wallenberg Foundation, 570630‐3095
Available from: 2023-04-19 Created: 2023-04-19 Last updated: 2023-09-07Bibliographically approved
Fridolfsson, E., Bunse, C., Lindehoff, E., Farnelid, H., Pontiller, B., Bergström, K., . . . Hylander, S. (2023). Multiyear analysis uncovers coordinated seasonality in stocks and composition of the planktonic food web in the Baltic Sea proper. Scientific Reports, 13(1), Article ID 11865.
Open this publication in new window or tab >>Multiyear analysis uncovers coordinated seasonality in stocks and composition of the planktonic food web in the Baltic Sea proper
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2023 (English)In: Scientific Reports, E-ISSN 2045-2322, Vol. 13, no 1, article id 11865Article in journal (Refereed) Published
Abstract [en]

The planktonic realm from bacteria to zooplankton provides the baseline for pelagic aquatic food webs. However, multiple trophic levels are seldomly included in time series studies, hampering a holistic understanding of the influence of seasonal dynamics and species interactions on food web structure and biogeochemical cycles. Here, we investigated plankton community composition, focusing on bacterio-, phyto- and large mesozooplankton, and how biotic and abiotic factors correlate at the Linnaeus Microbial Observatory (LMO) station in the Baltic Sea from 2011 to 2018. Plankton communities structures showed pronounced dynamic shifts with recurring patterns. Summarizing the parts of the planktonic microbial food web studied here to total carbon, a picture emerges with phytoplankton consistently contributing > 39% while bacterio- and large mesozooplankton contributed ~ 30% and ~ 7%, respectively, during summer. Cyanophyceae, Actinobacteria, Bacteroidetes, and Proteobacteria were important groups among the prokaryotes. Importantly, Dinophyceae, and not Bacillariophyceae, dominated the autotrophic spring bloom whereas Litostomatea (ciliates) and Appendicularia contributed significantly to the consumer entities together with the more traditionally observed mesozooplankton, Copepoda and Cladocera. Our findings of seasonality in both plankton composition and carbon stocks emphasize the importance of time series analyses of food web structure for characterizing the regulation of biogeochemical cycles and appropriately constraining ecosystem models. 

Place, publisher, year, edition, pages
Springer Nature, 2023
National Category
Oceanography, Hydrology and Water Resources Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-123829 (URN)10.1038/s41598-023-38816-0 (DOI)001124173100020 ()2-s2.0-85165356529 (Scopus ID)
Available from: 2023-08-21 Created: 2023-08-21 Last updated: 2024-02-06Bibliographically approved
Verma, A., Amnebrink, D., Pinhassi, J. & Wikner, J. (2023). Prokaryotic maintenance respiration and growth efficiency field patterns reproduced by temperature and nutrient control at mesocosm scale. Environmental Microbiology, 25(3), 721-737
Open this publication in new window or tab >>Prokaryotic maintenance respiration and growth efficiency field patterns reproduced by temperature and nutrient control at mesocosm scale
2023 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 25, no 3, p. 721-737Article in journal (Refereed) Published
Abstract [en]

The distribution of prokaryotic metabolism between maintenance and growth activities has a profound impact on the transformation of carbon substrates to either biomass or CO2. Knowledge of key factors influencing prokaryotic maintenance respiration is, however, highly limited. This mesocosm study validated the significance of prokaryotic maintenance respiration by mimicking temperature and nutrients within levels representative of winter and summer conditions. A global range of growth efficiencies (0.05-0.57) and specific growth rates (0.06-2.7 d(-1)) were obtained. The field pattern of cell-specific respiration versus specific growth rate and the global relationship between growth efficiency and growth rate were reproduced. Maintenance respiration accounted for 75% and 15% of prokaryotic respiration corresponding to winter and summer conditions, respectively. Temperature and nutrients showed independent positive effects for all prokaryotic variables except abundance and cell-specific respiration. All treatments resulted in different taxonomic diversity, with specific populations of amplicon sequence variants associated with either maintenance or growth conditions. These results validate a significant relationship between specific growth and respiration rate under productive conditions and show that elevated prokaryotic maintenance respiration can occur under cold and oligotrophic conditions. The experimental design provides a tool for further study of prokaryotic energy metabolism under realistic conditions at the mesocosm scale.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
National Category
Ecology Microbiology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-118752 (URN)10.1111/1462-2920.16300 (DOI)000905378800001 ()36511634 (PubMedID)2-s2.0-85145287538 (Scopus ID)
Available from: 2023-01-26 Created: 2023-01-26 Last updated: 2023-05-10Bibliographically approved
Massing, J. C., Fahimipour, A. K. K., Bunse, C., Pinhassi, J. & Gross, T. (2023). Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community. mSystems, 8(3), Article ID e00028-23.
Open this publication in new window or tab >>Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
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2023 (English)In: mSystems, E-ISSN 2379-5077, Vol. 8, no 3, article id e00028-23Article in journal (Refereed) Published
Abstract [en]

The increase in data availability of bacterial communities highlights the need for conceptual frameworks to advance our understanding of these complex and diverse communities alongside the production of such data. To understand the dynamics of these tremendously diverse communities, we need tools to identify overarching strategies and describe their role and function in the ecosystem in a comprehensive way. Here, we show that a manifold learning approach can coarse grain bacterial communities in terms of their metabolic strategies and that we can thereby quantitatively organize genomic information in terms of potentially occupied niches over time. This approach therefore advances our understanding of how fluctuations in bacterial abundances and species composition can relate to ecosystem functions and it can facilitate the analysis, monitoring and future predictions of the development of microbial communities. Progress in molecular methods has enabled the monitoring of bacterial populations in time. Nevertheless, understanding community dynamics and its links with ecosystem functioning remains challenging due to the tremendous diversity of microorganisms. Conceptual frameworks that make sense of time-series of taxonomically-rich bacterial communities, regarding their potential ecological function, are needed. A key concept for organizing ecological functions is the niche, the set of strategies that enable a population to persist and define its impacts on the surroundings. Here we present a framework based on manifold learning, to organize genomic information into potentially occupied bacterial metabolic niches over time. Manifold learning tries to uncover low-dimensional data structures in high-dimensional datasets, that can be used to describe the data in reduced dimensions. We apply the method to re-construct the dynamics of putatively occupied metabolic niches using a long-term bacterial time-series from the Baltic Sea, the Linnaeus Microbial Observatory (LMO). The results reveal a relatively low-dimensional space of occupied metabolic niches comprising groups of taxa with similar functional capabilities. Time patterns of occupied niches were strongly driven by seasonality. Some metabolic niches were dominated by one bacterial taxon whereas others were occupied by multiple taxa, depending on season. These results illustrate the power of manifold learning approaches to advance our understanding of the links between community composition and functioning in microbial systems.IMPORTANCEThe increase in data availability of bacterial communities highlights the need for conceptual frameworks to advance our understanding of these complex and diverse communities alongside the production of such data. To understand the dynamics of these tremendously diverse communities, we need tools to identify overarching strategies and describe their role and function in the ecosystem in a comprehensive way. Here, we show that a manifold learning approach can coarse grain bacterial communities in terms of their metabolic strategies and that we can thereby quantitatively organize genomic information in terms of potentially occupied niches over time. This approach therefore advances our understanding of how fluctuations in bacterial abundances and species composition can relate to ecosystem functions and it can facilitate the analysis, monitoring and future predictions of the development of microbial communities.

Place, publisher, year, edition, pages
American Society for Microbiology, 2023
Keywords
niche, marine, manifold learning, diffusion map, bacterial communities
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-123595 (URN)10.1128/msystems.00028-23 (DOI)001026287200001 ()37255288 (PubMedID)2-s2.0-85164232970 (Scopus ID)
Available from: 2023-08-10 Created: 2023-08-10 Last updated: 2023-09-07Bibliographically approved
Abreu, C. I., Dal Bello, M., Bunse, C., Pinhassi, J. & Gore, J. (2023). Warmer temperatures favor slower-growing bacteria in natural marine communities. Science Advances, 9(19), Article ID 26eade8352.
Open this publication in new window or tab >>Warmer temperatures favor slower-growing bacteria in natural marine communities
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2023 (English)In: Science Advances, E-ISSN 2375-2548, Vol. 9, no 19, article id 26eade8352Article in journal (Refereed) Published
Abstract [en]

Earth's life-sustaining oceans harbor diverse bacterial communities that display varying composition across time and space. While particular patterns of variation have been linked to a range of factors, unifying rules are lacking, preventing the prediction of future changes. Here, analyzing the distribution of fast- and slowgrowing bacteria in ocean datasets spanning seasons, latitude, and depth, we show that higher seawater temperatures universally favor slower-growing taxa, in agreement with theoretical predictions of how temperaturedependent growth rates differentially modulate the impact of mortality on species abundances. Changes in bacterial community structure promoted by temperature are independent of variations in nutrients along spatial and temporal gradients. Our results help explain why slow growers dominate at the ocean surface, during summer, and near the tropics and provide a framework to understand how bacterial communities will change in a warmer world.

Place, publisher, year, edition, pages
American Association for the Advancement of Science (AAAS), 2023
National Category
Ecology Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-123536 (URN)10.1126/sciadv.ade8352 (DOI)001004504000021 ()37163596 (PubMedID)2-s2.0-85158856368 (Scopus ID)
Available from: 2023-08-09 Created: 2023-08-09 Last updated: 2023-09-07Bibliographically approved
Westmeijer, G., Mehrshad, M., Turner, S., Alakangas, L., Sachpazidou, V., Bunse, C., . . . Dopson, M. (2022). Connectivity of Fennoscandian Shield terrestrial deep biosphere microbiomes with surface communities. Communications Biology, 5(1), Article ID 37.
Open this publication in new window or tab >>Connectivity of Fennoscandian Shield terrestrial deep biosphere microbiomes with surface communities
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2022 (English)In: Communications Biology, E-ISSN 2399-3642, Vol. 5, no 1, article id 37Article in journal (Refereed) Published
Abstract [en]

The deep biosphere is an energy constrained ecosystem yet fosters diverse microbial communities that are key in biogeochemical cycling. Whether microbial communities in deep biosphere groundwaters are shaped by infiltration of allochthonous surface microorganisms or the evolution of autochthonous species remains unresolved. In this study, 16S rRNA gene amplicon analyses showed that few groups of surface microbes infiltrated deep biosphere groundwaters at the Äspö Hard Rock Laboratory, Sweden, but that such populations constituted up to 49% of the microbial abundance. The dominant persisting phyla included Patescibacteria, Proteobacteria, and Epsilonbacteraeota. Despite the hydrological connection of the Baltic Sea with the studied groundwaters, infiltrating microbes predominantly originated from deep soil groundwater. Most deep biosphere groundwater populations lacked surface representatives, suggesting that they have evolved from ancient autochthonous populations. We propose that deep biosphere groundwater communities in the Fennoscandian Shield consist of selected infiltrated and indigenous populations adapted to the prevailing conditions.

Place, publisher, year, edition, pages
Nature Publishing Group, 2022
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-109214 (URN)10.1038/s42003-021-02980-8 (DOI)000741646700012 ()35017653 (PubMedID)2-s2.0-85122794173 (Scopus ID)2022 (Local ID)2022 (Archive number)2022 (OAI)
Funder
Swedish Research Council, 2018-04311
Available from: 2022-01-14 Created: 2022-01-14 Last updated: 2024-01-11Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-6405-1347

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