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  • 1.
    Bunse, Carina
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lundin, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Karlsson, Christofer M. G.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Akram, Neelam
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Vila-Costa, Maria
    Centre d’Estudis Avançats de Blanes-CSIC, Spain.
    Palovaara, Joakim
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Svensson, Lovisa
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    González, José M.
    University of La Laguna, Spain.
    Calvo, Eva
    Institut de Ciències del Mar—CSIC, Spain.
    Pelejero, Carles
    Institut de Ciències del Mar—CSIC, Spain.
    Marrasé, Cèlia
    Institut de Ciències del Mar—CSIC, Spain.
    Dopson, Mark
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Gasol, Josep
    Institut de Ciències del Mar—CSIC, Spain.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Response of marine bacterioplankton pH homeostasis gene expression to elevated CO22016In: Nature Climate Change, ISSN 1758-678X, E-ISSN 1758-6798, Vol. 6, no 5, p. 483-487Article in journal (Refereed)
    Abstract [en]

    Human-induced ocean acidification impacts marine life. Marine bacteria are major drivers of biogeochemical nutrient cycles and energy fluxes1; hence, understanding their performance under projected climate change scenarios is crucial for assessing ecosystem functioning. Whereas genetic and physiological responses of phytoplankton to ocean acidification are being disentangled2, 3, 4, corresponding functional responses of bacterioplankton to pH reduction from elevated CO2 are essentially unknown. Here we show, from metatranscriptome analyses of a phytoplankton bloom mesocosm experiment, that marine bacteria responded to lowered pH by enhancing the expression of genes encoding proton pumps, such as respiration complexes, proteorhodopsin and membrane transporters. Moreover, taxonomic transcript analysis showed that distinct bacterial groups expressed different pH homeostasis genes in response to elevated CO2. These responses were substantial for numerous pH homeostasis genes under low-chlorophyll conditions (chlorophyll a <2.5 μg l−1); however, the changes in gene expression under high-chlorophyll conditions (chlorophyll a >20 μg l−1) were low. Given that proton expulsion through pH homeostasis mechanisms is energetically costly, these findings suggest that bacterioplankton adaptation to ocean acidification could have long-term effects on the economy of ocean ecosystems.

  • 2.
    Holmfeldt, Karin
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Dziallas, Claudia
    Titelman, Josefin
    Pohlmann, Kirsten
    Grossart, Hans-Peter
    Riemann, Lasse
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Diversity and abundance of freshwater Actinobacteria along environmental gradients in the brackish northern Baltic Sea2009In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 11, no 8, p. 2042-2054Article in journal (Refereed)
    Abstract [en]

    Actinobacteria are highly abundant in pelagic freshwater habitats and also occur in estuarine environments such as the Baltic Sea. Because of gradients in salinity and other environmental variables estuaries offer natural systems for examining factors that determine Actinobacteria distribution. We studied abundance and community structure of Bacteria and Actinobacteria along two transects in the northern Baltic Sea. Quantitative (CARD-FISH) and qualitative (DGGE and clone libraries) analyses of community composition were compared with environmental parameters. Actinobacteria accounted for 22-27% of all bacteria and the abundance changed with temperature. Analysis of 549 actinobacterial 16S rRNA sequences from four clone libraries revealed a dominance of the freshwater clusters acI and acIV, and two new subclusters (acI-B scB-5 and acIV-E) were assigned. Whereas acI was present at all stations, occurrence of acII and acIV differed between stations and was related to dissolved organic carbon (DOC) and chlorophyll a (Chl a) respectively. The prevalence of the acI-A and acI-B subclusters changed in relation to total phosphorus (Tot-P) and Chl a respectively. Community structure of Bacteria and Actinobacteria differed between the river station and all other stations, responding to differences in DOC, Chl a and bacterial production. In contrast, the composition of active Actinobacteria (analysis based on reversely transcribed RNA) changed in relation to salinity and Tot-P. Our study suggests an important ecological role of Actinobacteria in the brackish northern Baltic Sea. It highlights the need to address dynamics at the cluster or subcluster phylogenetic levels to gain insights into the factors regulating distribution and composition of Actinobacteria in aquatic environments.

  • 3.
    Holmfeldt, Karin
    et al.
    University of Arizona, USA.
    Howard-Varona, Cristina
    University of Arizona, USA.
    Solonenko, Natalie
    University of Arizona, USA.
    Sullivan, Matthew B
    University of Arizona, USA.
    Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera2014In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 16, no 8, p. 2501-2513Article in journal (Refereed)
    Abstract [en]

    Bacterial viruses (phages) are abundant, ecologically important biological entities. However, our understanding of their impact is limited by model systems that are primarily not well represented in nature, e.g. Enterophages and their hosts. Here, we investigate genomic characteristics and infection strategies among six aquatic Bacteroidetes phages that represent two genera of exceptionally large (∼70-75 kb genome) podoviruses, which were isolated from the same seawater sample using Cellulophaga baltica as host. Quantitative host range studies reveal that these genera have contrasting narrow (specialist) and broad (generalist) host ranges, with one-step growth curves revealing reduced burst sizes for the generalist phages. Genomic comparisons suggest candidate genes in each genus that might explain this host range variation, as well as provide hypotheses about receptors in the hosts. One generalist phage, φ38:1, was more deeply characterized, as its infection strategy switched from lytic on its original host to either inefficient lytic or lysogenic on an alternative host. If lysogenic, this phage was maintained extrachromosomally in the alternative host and could not be induced by mitomycin C. This work provides fundamental knowledge regarding phage-host ranges and their genomic drivers while also exploring the 'host environment' as a driver for switching phage replication mode.

  • 4.
    Holmfeldt, Karin
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Middelboe, Mathias
    Nybroe, Ole
    Riemann, Lasse
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts2007In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 73, p. 6730-6739Article in journal (Refereed)
  • 5.
    Holmfeldt, Karin
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Odić, Duško
    Sullivan, Matthew B
    Middelboe, Mathias
    Riemann, Lasse
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains.2012In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 78, no 3, p. 892-894Article in journal (Refereed)
    Abstract [en]

    This is the first description of cultivated icosahedral single-stranded DNA (ssDNA) phages isolated on heterotrophic marine bacterioplankton and with Bacteroidetes hosts. None of the 8 phages stained well with DNA-binding stains, suggesting that in situ abundances of ssDNA phages are drastically underestimated using conventional methods for enumeration.

  • 6.
    Holmfeldt, Karin
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Arizona, USA.
    Solonenko, Natalie
    Univ Arizona, USA;Ohio State Univ, USA.
    Howard-Varona, Cristina
    Univ Arizona, USA;Ohio State Univ, USA.
    Moreno, Mario
    Univ Arizona, USA.
    Malmstrom, Rex R.
    DOE Joint Genome Inst, USA.
    Blow, Matthew J.
    DOE Joint Genome Inst, USA.
    Sullivan, Matthew B.
    Univ Arizona, USA;Ohio State Univ, USA.
    Large-scale maps of variable infection efficiencies in aquatic Bacteroidetes phage-host model systems2016In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 18, no 11, p. 3949-3961Article in journal (Refereed)
    Abstract [en]

    Microbes drive ecosystem functioning and their viruses modulate these impacts through mortality, gene transfer and metabolic reprogramming. Despite the importance of virus-host interactions and likely variable infection efficiencies of individual phages across hosts, such variability is seldom quantified. Here, we quantify infection efficiencies of 38 phages against 19 host strains in aquatic Cellulophaga (Bacteroidetes) phage-host model systems. Binary data revealed that some phages infected only one strain while others infected 17, whereas quantitative data revealed that efficiency of infection could vary 10 orders of magnitude, even among phages within one population. This provides a baseline for understanding and modeling intrapopulation host range variation. Genera specific host ranges were also informative. For example, the Cellulophaga Microviridae, showed a markedly broader intra-species host range than previously observed in Escherichia coli systems. Further, one phage genus, Cba41, was examined to investigate nonheritable changes in plating efficiency and burst size that depended on which host strain it most recently infected. While consistent with host modification of phage DNA, no differences in nucleotide sequence or DNA modifications were detected, leaving the observation repeatable, but the mechanism unresolved. Overall, this study highlights the importance of quantitatively considering replication variations in studies of phage-host interactions.

  • 7.
    Holmfeldt, Karin
    et al.
    Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721.
    Solonenko, Natalie
    Shah, Manesh
    Corrier, Kristen
    Riemann, Lasse
    Department of Biology, University of Copenhagen, 3000 Helsingor, Denmark.
    VerBerkmoes, Nathan C.
    Sullivan, Matthew B.
    Twelve previously unknown phage genera are ubiquitous in global oceans2013In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 110, no 31, p. 12798-12803Article in journal (Refereed)
    Abstract [en]

    Viruses are fundamental to ecosystems ranging from oceans to humans, yet our ability to study them is bottlenecked by the lack of ecologically relevant isolates, resulting in "unknowns" dominating culture-independent surveys. Here we present genomes from 31 phages infecting multiple strains of the aquatic bacterium Cellulophaga baltica (Bacteroidetes) to provide data for an under-represented and environmentally abundant bacterial lineage. Comparative genomics delineated 12 phage groups that (i) each represent a new genus, and (ii) represent one novel and four well-known viral families. This diversity contrasts the few well-studied marine phage systems, but parallels the diversity of phages infecting human-associated bacteria. Although all 12 Cellulophaga phages represent new genera, the podoviruses and icosahedral, nontailed ssDNA phages were exceptional, with genomes up to twice as large as those previously observed for each phage type. Structural novelty was also substantial, requiring experimental phage proteomics to identify 83% of the structural proteins. The presence of uncommon nucleotide metabolism genes in four genera likely underscores the importance of scavenging nutrient-rich molecules as previously seen for phages in marine environments. Metagenomic recruitment analyses suggest that these particular Cellulophaga phages are rare and may represent a first glimpse into the phage side of the rare biosphere. However, these analyses also revealed that these phage genera are widespread, occurring in 94% of 137 investigated metagenomes. Together, this diverse and novel collection of phages identifies a small but ubiquitous fraction of unknown marine viral diversity and provides numerous environmentally relevant phage-host systems for experimental hypothesis testing.

  • 8.
    Holmfeldt, Karin
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Titelman, Josefin
    University of Gothenburg ; University of Oslo.
    Riemann, Lasse
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Virus production and lysate recycling in different sub-basins of the northern Baltic Sea.2010In: Microbial Ecology, ISSN 0095-3628, E-ISSN 1432-184X, Vol. 60, no 3, p. 572-580Article in journal (Refereed)
    Abstract [en]

    In the Gulf of Bothnia, northern Baltic Sea, a large freshwater inflow creates north-southerly gradients in physico-chemical and biological factors across the two sub-basins, the Bothnian Bay (BB) and the Bothnian Sea. In particular, the sub-basins differ in nutrient limitation (nitrogen vs. phosphorus; P). Since viruses are rich in P, and virus production is commonly connected with bacterial abundance and growth, we hypothesized that the role of viral lysis differs between the sub-basins. Thus, we examined virus production and the potential importance of lysate recycling in surface waters along a transect in the Gulf of Bothnia. Surprisingly, virus production and total P were negatively correlated. In the BB, virus production rates were double those elsewhere in the system, although bacterial abundance and production were the lowest. In the BB, virus-mediated cell lysates could account for 70-180% and 100-250% of the bacterial carbon and P demand, respectively, while only 4-15% and 8-21% at the other stations. Low concentrations of dissolved DNA (D-DNA) with a high proportion of encapsulated DNA (viruses) in the BB suggested rapid turnover and high uptake of free DNA. The correlation of D-DNA and total P indicates that D-DNA is a particularly important nutrient source in the P-limited BB. Our study demonstrates large and counterintuitive differences in virus-mediated recycling of carbon and nutrients in two basins of the Gulf of Bothnia, which differ in microbial community composition and nutrient limitation.

  • 9.
    Howard-Varona, Cristina
    et al.
    University of Arizona, USA.
    Roux, Simon
    University of Arizona, USA.
    Dore, Hugo
    École normale supérieure de Lyon, France.
    Solonenko, Natalie E
    University of Arizona, USA.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Markillie, Lye M
    Pacific Northwest National Laboratory, USA.
    Orr, Galya
    Pacific Northwest National Laboratory, USA.
    Sullivan, Matthew B
    University of Arizona, USA.
    Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus.2017In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 11, no 1, p. 284-295Article in journal (Refereed)
    Abstract [en]

    Bacteria impact humans, industry and nature, but do so under viral constraints. Problematically, knowledge of viral infection efficiencies and outcomes derives from few model systems that over-represent efficient lytic infections and under-represent virus-host natural diversity. Here we sought to understand infection efficiency regulation in an emerging environmental Bacteroidetes-virus model system with markedly different outcomes on two genetically and physiologically nearly identical host strains. For this, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout both infections. While phage transcriptomes were similar, transcriptional differences between hosts suggested host-derived regulation of infection efficiency. Specifically, the alternative host overexpressed DNA degradation genes and underexpressed translation genes, which seemingly targeted phage DNA particle production, as experiments revealed they were both significantly delayed (by >30 min) and reduced (by >50%) in the inefficient infection. This suggests phage failure to repress early alternative host expression and stress response allowed the host to respond against infection by delaying phage DNA replication and protein translation. Given that this phage type is ubiquitous and abundant in the global oceans and that variable viral infection efficiencies are central to dynamic ecosystems, these data provide a critically needed foundation for understanding and modeling viral infections in nature.

  • 10.
    Lara, Elena
    et al.
    Institut de Ciències del Mar (CSIC), Spain.
    Holmfeldt, Karin
    University of Arizona, USA.
    Solonenko, Natalie
    University of Arizona, USA.
    Sà, Elisabet Laia
    Institut de Ciències del Mar (CSIC), Spain.
    Ignacio-Espinoza, J Cesar
    University of Arizona, USA.
    Cornejo-Castillo, Francisco M
    Institut de Ciències del Mar (CSIC), Spain.
    Verberkmoes, Nathan C
    Oak Ridge National Laboratory, USA.
    Vaqué, Dolors
    Institut de Ciències del Mar (CSIC), Spain.
    Sullivan, Matthew B
    University of Arizona, USA.
    Acinas, Silvia G
    Institut de Ciències del Mar (CSIC), Spain.
    Life-style and genome structure of marine Pseudoalteromonas siphovirus B8b isolated from the northwestern Mediterranean Sea.2015In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 1, article id e0114829Article in journal (Refereed)
    Abstract [en]

    Marine viruses (phages) alter bacterial diversity and evolution with impacts on marine biogeochemical cycles, and yet few well-developed model systems limit opportunities for hypothesis testing. Here we isolate phage B8b from the Mediterranean Sea using Pseudoalteromonas sp. QC-44 as a host and characterize it using myriad techniques. Morphologically, phage B8b was classified as a member of the Siphoviridae family. One-step growth analyses showed that this siphovirus had a latent period of 70 min and released 172 new viral particles per cell. Host range analysis against 89 bacterial host strains revealed that phage B8b infected 3 Pseudoalteromonas strains (52 tested, >99.9% 16S rRNA gene nucleotide identity) and 1 non-Pseudoaltermonas strain belonging to Alteromonas sp. (37 strains from 6 genera tested), which helps bound the phylogenetic distance possible in a phage-mediated horizontal gene transfer event. The Pseudoalteromonas phage B8b genome size was 42.7 kb, with clear structural and replication modules where the former were delineated leveraging identification of 16 structural genes by virion structural proteomics, only 4 of which had any similarity to known structural proteins. In nature, this phage was common in coastal marine environments in both photic and aphotic layers (found in 26.5% of available viral metagenomes), but not abundant in any sample (average per sample abundance was 0.65% of the reads). Together these data improve our understanding of siphoviruses in nature, and provide foundational information for a new 'rare virosphere' phage-host model system.

  • 11.
    Loderer, Christoph
    et al.
    Tech Univ Dresden, Germany.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lundin, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Stockholm University, Sweden.
    Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction2019In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 7, p. 1-17, article id e6700Article in journal (Refereed)
    Abstract [en]

    Ribonucleotide reductases (RNR) are essential enzymes for all known life forms. Their current taxonomic distribution suggests extensive horizontal gene transfer e.g., by processes involving viruses. To improve our understanding of the underlying processes, we characterized a monomeric class II RNR (NrdJm) enzyme from a Thermus virus, a subclass not present in any sequenced Thermus spp. genome. Phylogenetic analysis revealed a distant origin of the nrdJm gene with the most closely related sequences found in mesophiles or moderate thermophiles from the Firmicutes phylum. GC-content, codon usage and the ratio of coding to non-coding substitutions (dN/dS) suggest extensive adaptation of the gene in the virus in terms of nucleotide composition and amino acid sequence. The NrdJm enzyme is a monomeric B-12-dependent RNR with nucleoside triphosphate specificity. It exhibits a temperature optimum at 60-70 degrees C, which is in the range of the growth optimum of Thermus spp. Experiments in combination with the Thermus thermophilus thioredoxin system show that the enzyme is able to retrieve electrons from the host NADPH pool via host thioredoxin and thioredoxin reductases. This is different from other characterized viral RNRs such as T4 phage RNR, where a viral thioredoxin is present. We hence show that the monomeric class II RNR, present in Thermus viruses, was likely transferred from an organism phylogenetically distant from the one they were isolated from, and adapted to the new host in genetic signature and amino acids sequence.

  • 12.
    Lopez-Fernandez, Margarita
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Helmholtz Zentrum, Germany.
    Simone, Domenico
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wu, Xiaofen
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Soler, Lucile
    Uppsala University.
    Nilsson, Emelie
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lantz, Henrik
    Uppsala University.
    Bertilsson, Stefan
    Uppsala University.
    Dopson, Mark
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere2018In: mBio, ISSN 2161-2129, E-ISSN 2150-7511, Vol. 9, no 6, article id e01792-18Article in journal (Refereed)
    Abstract [en]

    The continental subsurface is suggested to contain a significant part of the earth's total biomass. However, due to the difficulty of sampling, the deep subsurface is still one of the least understood ecosystems. Therefore, microorganisms inhabiting this environment might profoundly influence the global nutrient and energy cycles. In this study, in situ fixed RNA transcripts from two deep continental groundwaters from the Aspo Hard Rock Laboratory (a Baltic Sea-influenced water with a residence time of <20 years, defined as "modern marine," and an "old saline" groundwater with a residence time of thousands of years) were subjected to metatranscriptome sequencing. Although small subunit (SSU) rRNA gene and mRNA transcripts aligned to all three domains of life, supporting activity within these community subsets, the data also suggested that the groundwaters were dominated by bacteria. Many of the SSU rRNA transcripts grouped within newly described candidate phyla or could not be mapped to known branches on the tree of life, suggesting that a large portion of the active biota in the deep biosphere remains unexplored. Despite the extremely oligotrophic conditions, mRNA transcripts revealed a diverse range of metabolic strategies that were carried out by multiple taxa in the modern marine water that is fed by organic carbon from the surface. In contrast, the carbon dioxide- and hydrogen-fed old saline water with a residence time of thousands of years predominantly showed the potential to carry out translation. This suggested these cells were active, but waiting until an energy source episodically becomes available. IMPORTANCE A newly designed sampling apparatus was used to fix RNA under in situ conditions in the deep continental biosphere and benchmarks a strategy for deep biosphere metatranscriptomic sequencing. This apparatus enabled the identification of active community members and the processes they carry out in this extremely oligotrophic environment. This work presents for the first time evidence of eukaryotic, archaeal, and bacterial activity in two deep subsurface crystalline rock groundwaters from the Aspo Hard Rock Laboratory with different depths and geochemical characteristics. The findings highlight differences between organic carbonfed shallow communities and carbon dioxide- and hydrogen-fed old saline waters. In addition, the data reveal a large portion of uncharacterized microorganisms, as well as the important role of candidate phyla in the deep biosphere, but also the disparity in microbial diversity when using standard microbial 165 rRNA gene amplification versus the large unknown portion of the community identified with unbiased metatranscriptomes.

  • 13. Middelboe, Mathias
    et al.
    Holmfeldt, Karin
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Riemann, Lasse
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Nybroe, Ole
    Haaber, Jakob
    Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties2009In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 11, no 8, p. 1971-1982Article in journal (Refereed)
    Abstract [en]

    Genetic, structural and physiological differences between strains of the marine bacterium Cellulophaga baltica MM#3 (Flavobacteriaceae) developing in response to the activity of two virulent bacteriophages, Theta S(M) and Theta S(T), was investigated during 3 weeks incubation in chemostat cultures. A distinct strain succession towards increased phage resistance and a diversification of the metabolic properties was observed. During the incubation the bacterial population diversified from a single strain, which was sensitive to 24 tested Cellulophaga phages, into a multistrain and multiresistant population, where the dominant strains had lost susceptibility to up to 22 of the tested phages. By the end of the experiment the cultures reached a quasi steady state dominated by Theta S(T)-resistant and Theta S(M) + Theta S(T)-resistant strains coexisting with small populations of phage-sensitive strains sustaining both phages at densities of > 10(6) plaque forming units (pfu) ml(-1). Loss of susceptibility to phage infection was associated with a reduction in the strains' ability to metabolize various carbon sources as demonstrated by BIOLOG assays. This suggested a cost of resistance in terms of reduced physiological capacity. However, there was no direct correlation between the degree of resistance and the loss of metabolic properties, suggesting either the occurrence of compensatory mutations in successful strains or that the cost of resistance in some strains was associated with properties not resolved by the BIOLOG assay. The study represents the first direct demonstration of phage-driven generation of functional diversity within a marine bacterial host population with significant implications for both phage susceptibility and physiological properties. We propose, therefore, that phage-mediated selection for resistant strains contributes significantly to the extensive microdiversity observed within specific bacterial species in marine environments.

  • 14.
    Nilsson, Emelie
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Li, K.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Fridlund, Jimmy
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Sulcius, S.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Nat Res Ctr, Lithuania.
    Bunse, Carina
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Helmholtz Zentrum Polar & Meeresforsch, Germany;Carl von Ossietzky Univ Oldenburg, Germany.
    Karlsson, Christofer M. G.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lindh, Markus V.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Swedish Meteorological and Hydrological Institute, Sweden.
    Lundin, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL3412019In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 85, no 18, p. 1-19, article id e01003-19Article in journal (Refereed)
    Abstract [en]

    Knowledge in aquatic virology has been greatly improved by culture-independent methods, yet there is still a critical need for isolating novel phages to identify the large proportion of "unknowns" that dominate metagenomes and for detailed analyses of phage-host interactions. Here, 54 phages infecting Rheinheimem sp. strain BAL341 (Gammaproteobacteria) were isolated from Baltic Sea seawater and characterized through genome content analysis and comparative genomics. The phages showed a myovirus-like morphology and belonged to a novel genus, for which we propose the name Barbavirus. All phages had similar genome sizes and numbers of genes (80 to 84 kb; 134 to 145 genes), and based on average nucleotide identity and genome BLAST distance phylogeny, the phages were divided into five species. The phages possessed several genes involved in metabolic processes and host signaling, such as genes encoding ribonucleotide reductase and thymidylate synthase, phoH, and rnazG. One species had additional metabolic genes involved in pyridine nucleotide salvage, possibly providing a fitness advantage by further increasing the phages' replication efficiency. Recruitment of viral metagenomic reads (25 Baltic Sea viral metagenomes from 2012 to 2015) to the phage genomes showed pronounced seasonal variations, with increased relative abundances of barba phages in August and September synchronized with peaks in host abundances, as shown by 16S rRNA gene amplicon sequencing. Overall, this study provides detailed information regarding genetic diversity, phage-host interactions, and temporal dynamics of an ecologically important aquatic phage-host system. IMPORTANCE Phages are important in aquatic ecosystems as they influence their microbial hosts through lysis, gene transfer, transcriptional regulation, and expression of phage metabolic genes. Still, there is limited knowledge of how phages interact with their hosts, especially at fine scales. Here, a Rheinheimera phage-host system constituting highly similar phages infecting one host strain is presented. This relatively limited diversity has previously been seen only when smaller numbers of phages have been isolated and points toward ecological constraints affecting the Rheinheimera phage diversity. The variation of metabolic genes among the species points toward various fitness advantages, opening up possibilities for future hypothesis testing. Phage-host dynamics monitored over several years point toward recurring "kill-the-winner" oscillations and an ecological niche fulfilled by this system in the Baltic Sea. Identifying and quantifying ecological dynamics of such phage-host model systems in situ allow us to understand and study the influence of phages on aquatic ecosystems.

  • 15.
    Riemann, Lasse
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Holmfeldt, Karin
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Titelman, Josefin
    Importance of viral lysis and dissolved DNA for bacterioplankton activity in a P-limited estuary, northern Baltic Sea2009In: Microbial Ecology, ISSN 0095-3628, E-ISSN 1432-184X, Vol. 57, no 2, p. 286-294Article in journal (Refereed)
    Abstract [en]

    Through lysis of bacterioplankton cells, viruses mediate an important, but poorly understood, pathway of carbon and nutrients from the particulate to the dissolved form. Via this activity, nutrient-rich cell lysates may become available to noninfected cells and support significant growth. However, the nutritional value of lysates for noninfected bacteria presumably depends on the prevailing nutrient limitation. In the present study, we examined dynamics of dissolved DNA (D-DNA) and viruses along a transect in the phosphorus (P)-limited A-re Estuary, northern Baltic Sea. We found that viruses were an important mortality factor for bacterioplankton and that their activity mediated a significant recycling of carbon and especially of P. Uptake of dissolved DNA accounted for up to 70% of the bacterioplankton P demand, and about a quarter of the D-DNA pool was supplied through viral lysis of bacterial cells. Generally, the importance of viral lysates and uptake of D-DNA was highest at the estuarine and offshore stations and was positively correlated with P limitation measured as alkaline phosphatase activity. Our results highlight the importance of viral activity for the internal recycling of principal nutrients and pinpoints D-DNA as a particularly relevant compound in microbial P dynamics.

  • 16.
    Riemann, Lasse
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Leitet, C.
    Pommier, T.
    Simu, K.
    Holmfeldt, Karin
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Larsson, U.
    Hagström, Åke
    University of Kalmar, School of Pure and Applied Natural Sciences.
    The Native Bacterioplankton Community in the Central Baltic Sea is Influenced by Freshwater Bacterial Species2008In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 74, p. 503-515Article in journal (Refereed)
  • 17. Simu, Karin
    et al.
    Holmfeldt, Karin
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Zweifel, Ulla Li
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Hagström, Åke
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Culturability and coexistence of colony forming and single cell marine bacterioplankton.2005In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 71, p. 4793-4800Article in journal (Refereed)
  • 18.
    Šulčius, Sigitas
    et al.
    Nat Res Ctr, Lithuania.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Viruses of microorganisms in the Baltic Sea: current state of research and perspectives2016In: Marine Biology Research, ISSN 1745-1000, E-ISSN 1745-1019, Vol. 12, no 2, p. 115-124Article in journal (Refereed)
    Abstract [en]

    This paper reviews the current state of research into viruses of microorganisms in the Baltic Sea. Field and experimental studies reveal the great phenotypic and genotypic variety of the Baltic Sea viruses and highlights the importance of phages in the Baltic Sea food-web dynamics. In total, 93 virus isolates from the Baltic Sea have been described, the genome sequence being available for 39 of these. However, these isolates were derived from only eight host species and, therefore, underrepresent the overall viral diversity in the Baltic Sea. The most studied group of viruses is bacteriophages that infect Bacteroidetes, whereas, by contrast, phages of Cyanobacteria, Proteobacteria and Actinobacteria, as well as algal viruses, have been investigated to a lesser extent. No reports on viruses infecting Baltic Sea fungi and archaea isolates have been reported to date. This paper also identifies gaps in our knowledge of the aquatic virology of the Baltic Sea and emphasizes the need for more comprehensive analysis of those viruses that occur in one of the world’s largest brackish water ecosystems.

  • 19.
    Sulcius, Sigitas
    et al.
    Nat Res Ctr, Lithuania.
    Mazur-Marzec, Hanna
    Univ Gdansk, Poland;Polish Acad Sci, Poland.
    Vitonyte, Irma
    Nat Res Ctr, Lithuania.
    Kvederaviciute, Kotryna
    MAP Kinase Resource, Switzerland;Vilnius Univ, Lithuania.
    Kuznecova, Jolita
    Nat Res Ctr, Lithuania.
    Simoliunas, Eugenijus
    Vilnius Univ, Lithuania.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Insights into cyanophage-mediated dynamics of nodularin and other non-ribosomal peptides in Nodularia spumigena2018In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 78, p. 69-74Article in journal (Refereed)
    Abstract [en]

    The effect of cyanophage infection and lysis on the dynamics of the hepatotoxin nodularin (NOD) and other nonribosomal peptides (NRPs) produced by cyanobacteria is poorly understood. In this study, changes in concentration of NOD and other NRPs during cyanophage infection of the filamentous cyanobacteria Nodularia spumigena were assessed using incubation experiments. Viral infection and lysis were associated with a significant reduction (93% at the 96 h post infection) of N. spumigena cell density. While no correlation between N. spumigena abundance and total concentration of NOD (ng mL(-1)) within the infected cells was observed, cellular NOD quota (ng cell(-1)) gradually increased in the remaining cyanophage resistant N. spumigena subpopulation. Lysis of N. spurnigena cells resulted in a substantial increase (>57 times) of dissolved NOD concentration in the culture medium. The relative concentration of other cyclic (anabaenopeptins) and linear (aeruginosins, spumigins) NRPs produced by N. spumigena also increased in response to cyanophage addition. This study highlights the importance of cyanophage infection on the population toxicity of filamentous cyanobacteria and demonstrates a significant contribution of virus-mediated cell lysis on the conversion of NOD from the particulate to dissolved phase.

  • 20.
    Sulcius, Sigitas
    et al.
    Nat Res Ctr, Lithuania.
    Simoliunas, Eugenijus
    Vilnius Univ, Lithuania.
    Alzbutas, Gediminas
    Nat Res Ctr, Lithuania;Thermo Fisher Sci Balt, Lithuania;Vilnius Univ, Lithuania.
    Gasiunas, Giedrius
    Vilnius Univ, Lithuania;CasZyme, Lithuania.
    Jauniskis, Vykintas
    Vilnius Univ, Lithuania;Univ Copenhagen, Denmark.
    Kuznecova, Jolita
    Nat Res Ctr, Lithuania.
    Miettinen, Sini
    Univ Helsinki, Finland.
    Nilsson, Emelie
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Meskys, Rolandas
    Vilnius Univ, Lithuania.
    Roine, Elina
    Univ Helsinki, Finland.
    Paskauskas, Ricardas
    Nat Res Ctr, Lithuania.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Genomic Characterization of Cyanophage vB_AphaS-CL131 Infecting Filamentous Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Reveals Novel Insights into Virus-Bacterium Interactions2019In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 85, no 1, article id UNSP e01311-18Article in journal (Refereed)
    Abstract [en]

    While filamentous cyanobacteria play a crucial role in food web dynamics and biogeochemical cycling of many aquatic ecosystems around the globe, the knowledge regarding the phages infecting them is limited. Here, we describe the complete genome of the virulent cyanophage vB_AphaS-CL131 (here, CL 131), a Siphoviridae phage that infects the filamentous diazotrophic bloom-forming cyanobacterium Aphanizomenon flos-aquae in the brackish Baltic Sea. CL 131 features a 112,793-bp double-stranded DNA (dsDNA) genome encompassing 149 putative open reading frames (ORFs), of which the majority (86%) lack sequence homology to genes with known functions in other bacteriophages or bacteria. Phylogenetic analysis revealed that CL 131 possibly represents a new evolutionary lineage within the group of cyanophages infecting filamentous cyanobacteria, which form a separate cluster from phages infecting unicellular cyanobacteria. CL 131 encodes a putative type V-U2 CRISPR-Cas system with one spacer (out of 10) targeting a DNA primase pseudogene in a cyanobacterium and a putative type II toxin-antitoxin system, consisting of a GNAT family N-acetyltransferase and a protein of unknown function containing the PRK09726 domain (characteristic of HipB antitoxins). Comparison of CL 131 proteins to reads from Baltic Sea and other available fresh- and brackish-water metagenomes and analysis of CRISPR-Cas arrays in publicly available A. flos-aquae genomes demonstrated that phages similar to CL 131 are present and dynamic in the Baltic Sea and share a common history with their hosts dating back at least several decades. In addition, different CRISPR-Cas systems within individual A. flos-aquae genomes targeted several sequences in the CL 131 genome, including genes related to virion structure and morphogenesis. Altogether, these findings revealed new genomic information for exploring viral diversity and provide a model system for investigation of virus-host interactions in filamentous cyanobacteria. IMPORTANCE The genomic characterization of novel cyanophage vB_AphaS-CL131 and the analysis of its genomic features in the context of other viruses, metagenomic data, and host CRISPR-Cas systems contribute toward a better understanding of aquatic viral diversity and distribution in general and of brackish-water cyanophages infecting filamentous diazotrophic cyanobacteria in the Baltic Sea in particular. The results of this study revealed previously undescribed features of cyanophage genomes (e.g., self-excising intein-containing putative dCTP deaminase and putative cyanophage-encoded CRISPR-Cas and toxin-antitoxin systems) and can therefore be used to predict potential interactions between bloom-forming cyanobacteria and their cyanophages.

  • 21. Titelman, Josefin
    et al.
    Riemann, Lasse
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Holmfeldt, Karin
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Nilsen, Trygve
    Copepod feeding stimulates bacterioplankton in a low phosphorus system2008In: Aquatic Biology, ISSN 1864-7782, E-ISSN 1864-7790, Vol. 2, p. 131-141Article in journal (Refereed)
  • 22.
    Wu, Xiaofen
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Hubalek, Valerie
    Uppsala University.
    Lundin, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Åström, Mats E.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Bertilsson, Stefan
    Uppsala University.
    Dopson, Mark
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations2016In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 10, no 5, p. 1192-1203Article in journal (Refereed)
    Abstract [en]

    Microorganisms in the terrestrial deep biosphere host up to 20% of the earth's biomass and are suggested to be sustained by the gases hydrogen and carbon dioxide. A metagenome analysis of three deep subsurface water types of contrasting age (from <20 to several thousand years) and depth (171 to 448 m) revealed phylogenetically distinct microbial community subsets that either passed or were retained by a 0.22 μm filter. Such cells of <0.22 μm would have been overlooked in previous studies relying on membrane capture. Metagenomes from the three water types were used for reconstruction of 69 distinct microbial genomes, each with >86% coverage. The populations were dominated by Proteobacteria, Candidate divisions, unclassified archaea and unclassified bacteria. The estimated genome sizes of the <0.22 μm populations were generally smaller than their phylogenetically closest relatives, suggesting that small dimensions along with a reduced genome size may be adaptations to oligotrophy. Shallow 'modern marine' water showed community members with a predominantly heterotrophic lifestyle. In contrast, the deeper, 'old saline' water adhered more closely to the current paradigm of a hydrogen-driven deep biosphere. The data were finally used to create a combined metabolic model of the deep terrestrial biosphere microbial community.

  • 23. Zweifel, Ulla Li
    et al.
    Hagström, Åke
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Thyrhaug, Runar
    Geels, Camilla
    Frohn, Lise Marie
    Skjoth, Carsten A.
    Karlson, Ulrich Gosewinkel
    High bacterial 16S rRNA gene diversity above the atmospheric boundary layer2012In: Aerobiologia, ISSN 0393-5965, E-ISSN 1573-3025, Vol. 28, no 4, p. 481-498Article in journal (Refereed)
    Abstract [en]

    The atmosphere is host to an omnipresent bacterial community that may influence fundamental atmospheric processes such as cloud formation and precipitation onset. Knowledge of this bacterial community is scarce, particularly in air masses relevant to cloud formation. Using a light aircraft, we sampled above the atmospheric boundary layer-that is, at heights at which cloud condensation occurs-over coastal areas of Sweden and Denmark in summer 2009. Enumeration indicated total bacterial numbers of 4 x 10(1) to 1.8 x 10(3) m(-3) air and colony-forming units of 0-6 bacteria m(-3) air. 16S rRNA gene libraries constructed from samples collected above the Baltic Sea coast revealed a highly diverse bacterial community dominated by species belonging to the genera Sphingomonas and Pseudomonas. Bacterial species known to carry ice-nucleating proteins were found in several samples. Modeled back trajectories suggested the potential sources of the sampled bacteria to be diverse geographic regions, including both marine and terrestrial environments in the northern hemisphere. Several samples contained 16S rRNA genes from plant chloroplasts, confirming a terrestrial contribution to these samples. Interestingly, the airborne bacterial community displayed an apparent seasonal succession that we tentatively ascribe to in situ succession in the atmosphere.

1 - 23 of 23
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