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Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Lnuc EEMiS)ORCID iD: 0000-0001-5103-214X
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Lnuc EEMiS)
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Lnuc EEMiS)
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Nat Res Ctr, Lithuania. (Lnuc EEMiS)ORCID iD: 0000-0002-2686-8348
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2019 (English)In: 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) Published
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.

Place, publisher, year, edition, pages
American Society for Microbiology , 2019. Vol. 85, no 18, p. 1-19, article id e01003-19
Keywords [en]
Baltic Sea, bacteriophage, genomics, temporal variation
National Category
Ecology Microbiology
Research subject
Ecology, Microbiology; Ecology, Aquatic Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-89282DOI: 10.1128/AEM.01003-19ISI: 000483596700008PubMedID: 31324626Scopus ID: 2-s2.0-85071782126OAI: oai:DiVA.org:lnu-89282DiVA, id: diva2:1354476
Available from: 2019-09-25 Created: 2019-09-25 Last updated: 2025-09-23Bibliographically approved
In thesis
1. Diversity of aquatic viruses from genes to host interactions
Open this publication in new window or tab >>Diversity of aquatic viruses from genes to host interactions
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Viruses are the most numerous entities on Earth, and can be found in all waters. In aquatic ecosystems, viruses are key players since they alter the way energy and nutrients are transferred by killing larger organisms. However, we still lack fundamental knowledge about aquatic viruses’ diversity, prevalence and in what ways and to what extant viruses influence their hosts. Therefore, I used laboratory and bioinformatic methods to investigate who these viruses are and in what ways they interact with their hosts.

Previously unknown viruses within the deep biosphere as well as in Baltic Sea surface water were characterised. Bioinformatic approaches were used to describe the entire viral community in three different waters from the deep biosphere. These viral communities turned out to be highly novel compared to what has previously been seen. Water from the Baltic Sea was used to isolate viruses (bacteriophages, phages in short) infecting select bacterial hosts, and 93 previously unknown phages, encompassing 21 novel species in seven genera, were described. All these newly discovered viruses suggest that our knowledge of viral diversity is far from complete and that further studies are needed.

By combining laboratory and bioinformatic methods, I disentangled who infected whom and was able to link this to abundance patterns in the wild. While the first part is important to recognise the potential of natural phage communities, the latter is key to understand what impact phages will have. Further, with a laboratory experiment I showed that phage infection could change the metabolism of the host, and that the changes were nutrient dependent. These studies highlight the importance of considering complex interactions to comprehend natural ecosystems.

Taken together, this thesis increases our knowledge regarding aquatic viruses’ diversity, their functions and host interactions, which is of great relevance when trying to understand the world around us and how it will change in the future. Viruses are diverse and active both in the deep biosphere and surface waters, they persist over time and they alter host metabolism. These findings provide novel insights into microbial aquatic ecology and highlights the importance of viruses.

Abstract [sv]

Virus är de talrikaste entiteterna på jorden och de finns i alla vatten. I dessa akvatiska ekosystem har virus en nyckelroll eftersom de påverkar på vilket sätt energi och näring förflyttas mellan olika nivåer i födoväven. Genom att infektera och döda encelliga organismer förhindrar de att näring förs upp till större organismer, istället förblir näringen tillgänglig till andra encelliga organismer. Trots att virus är viktiga, så saknar vi fortfarande grundläggande kunskap om akvatiska virus diversitet, deras utbredning och hur och till vilken grad virus påverkar sina värdar. Därför använde jag laboratorie- och bioinformatiska metoder för att undersöka vilka dessa virus är och hur de interagerar med sina värdar.

För att besvara vilka virus som finns i två̊ olika miljöer, den djupa biosfären och Östersjöns ytvatten, undersökte jag både DNA frän hela virussamhällen och isolerade virus som infekterar specifika bakterier. Med de bioinformatiska analyserna av hela virussamhällen kunde jag beskriva virusen som fanns i tre olika vatten i den djupa biosfären. Dessa visade sig vara annorlunda jämfört mot virussamhällen som har beskrivits tidigare. Vatten ifrån Östersjön användes för att isolera virus som infekterar specifika bakterier (bakteriofager, även kallade fager). Därigenom blev 93 tidigare okända fagtyper karaktäriserade och de placerades i 21 nya arter inom sju nya släkten. Förekomsten av alla dessa tidigare ökända virus visar på att vår kunskap om virus diversitet är långt ifrån komplett och att detta behöver studeras än mer.

För att studera hur virus interagerar med sina värdar använde jag en kombination av labb och bioinformatiska metoder. Detta gjorde att jag kunde reda ut vem som infekterade vem, och möjliggjorde att koppla detta till mönster av förekomst i akvatiska miljöer. Den första delen, vem som infekterar vem, är viktigt för att förstå vilken potential som finns i naturliga fagsamhällen, medan den andra delen är väsentlig för att begripa vilken betydelse fager har på̊ naturliga mikrobiella samhällen. Med labbexperiment kunde jag även visa att faginfektioner kan förändra bakterievärdens metabolism, och att dessa förändringar kan påverkas av mängden näring som bakterien växte i. De här studierna belyser vikten av att ha komplexa interaktioner i åtanke för att förstå naturliga ekosystem.

Sammanfattningsvis, den här avhandlingen ökar vår kunskap kring akvatiska virus diversitet, deras funktioner och hur de interagerar med sina värdar. Detta är viktigt när vi försöker förstå̊ världen runtomkring oss och hur den kommer att förändras i framtiden. Virus finns i många olika varianter och de är aktiva i både den djupa biosfären och i ytvatten, de förekommer över tid och förändrar sina värdars metabolism. De här fynden bidrar med insikter om mikrobiell akvatisk ekologi och visar på hur viktiga virus är.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2020. p. 49
Series
Linnaeus University Dissertations ; 387/2020
Keywords
microbial ecology, bacteriophage, ‘omics, isolation, host range, temporal variation, deep biosphere, Baltic Sea
National Category
Ecology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-97539 (URN)9789189081772 (ISBN)9789189081789 (ISBN)
Public defence
2020-09-04, Fullriggaren (Ma135), Hus Magna, Kalmar, 09:30 (English)
Opponent
Supervisors
Available from: 2020-08-13 Created: 2020-08-13 Last updated: 2025-02-26Bibliographically approved

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Nilsson, EmelieFridlund, JimmyŠulčius, SigitasBunse, CarinaKarlsson, Christofer M. G.Lindh, Markus V.Lundin, DanielPinhassi, JaroneHolmfeldt, Karin

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