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Genome-resolved analysis reveals transcriptional transitions across seasons in Baltic Sea prokaryotes
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.ORCID iD: 0000-0002-2747-6346
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.ORCID iD: 0000-0002-8779-6464
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Microbial communities in surface waters of temperate seas are exposed to recurring annual seasonal variation in temperature and nutrient concentrations. To what extent bacterioplankton populations in natural communities alter their functional repertoire as a result of seasonal succession has not been thoroughly investigated. Here we use metatranscriptomics and leverage a comprehensive catalogue of metagenome-assembled genomes (MAGs) to follow gene expression in individual populations over a two-year time period at an offshore station in the Baltic Sea. We show that the collective expression of the MAGs changed in a consistent manner across seasons in the two years, forming clusters representing the four seasons, and that more than 80% of these displayed a recurring seasonal pattern. Furthermore, we found that the changes in expression could partly be explained by modulation of expression within the prokaryotic populations, since intra-population expression patterns also changed with season. Taken together, our results demonstrate how natural microbial populations alter their expression on the gene level, and how these changes drive large scale changes on both population and community level. This work aims to broaden the understanding of how microbes respond and adapt to their environment by preferentially altering their expressed genetic repertoire, and how microbial community dynamics can be explained through the gene expression of various populations constituting the community. 

National Category
Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-129187OAI: oai:DiVA.org:lnu-129187DiVA, id: diva2:1856581
Available from: 2024-05-07 Created: 2024-05-07 Last updated: 2024-06-27
In thesis
1. Seasonality influences gene expression in Baltic Sea microbial communities
Open this publication in new window or tab >>Seasonality influences gene expression in Baltic Sea microbial communities
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Prokaryotes are the most abundant living organisms in the marine environment. They contribute to primary production and the recycling of its products. Collectively they influence the marine element cycles of carbon along with elements like nitrogen and sulfur. However, much remains to learn of the functional characteristics of microbial communities carrying out these processes, and how different communities respond to changing environmental conditions in space and time.The composition of marine prokaryotic communities is known to change in a seasonal manner, but how seasonality influences their gene expression or “activity” remains largely unknown. 

In this thesis I investigate the relationship between prokaryotic activity, relative gene expression, and seasonality using time series field data on gene expression combined with reference genomes of prokaryotic populations (metagenome assembled genomes, MAGs). This revealed pronounced seasonal succession in overall transcriptional dynamics. Importantly, roughly half of the 50 populations with highest relative abundance in transcription altered their transcriptional profiles across seasons. Thus, changes in relative gene expression on the annual scale is explained by community turnover and modulation of activity within populations. Characterization of a MAG representative of the filamentous cyanobacterial genus Aphanizomenon that forms summer blooms in the Baltic Proper, highlighted seasonal patterns in transcription of genes underlying key prokaryotic activities. This included genes related to photosynthesis (different genes expressed in different seasons), nitrogen- fixation (expression peaking in summer) and oxidative stress (peaking in winter). A mesocosm study in the Bothnian Sea using temperature and nutrient manipulations simulating the winter to summer transition showed lower growth efficiency and higher maintenance respiration in winter conditions, implying larger relative losses of CO2 through respiration in winter. Additionally, temperature, nutrients, and their combination, caused separation in both prokaryotic taxonomy and transcription of metabolic pathways. Key features included archaeal transcription of ammonium oxidation in winter conditions, and Oceanospirillales central metabolisms in summer. 

Taken together, these results highlight the pronounced effect of seasonality on prokaryotic community gene expression and the capability of prokaryotic populations to alter their expressed genetic repertoire. This emphasizes the importance of the temporal perspective when considering how prokaryotic communities will respond to changes in environmental conditions. 

Place, publisher, year, edition, pages
Linnaeus University Press, 2024. p. 42
Series
Linnaeus University Dissertations ; 526
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-129192 (URN)10.15626/LUD.526.2024 (DOI)9789180821605 (ISBN)9789180821599 (ISBN)
Public defence
2024-06-05, Sal Azur, Hus Vita, Kalmar, 09:00 (English)
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Supervisors
Available from: 2024-05-13 Created: 2024-05-07 Last updated: 2024-05-24Bibliographically approved

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Amnebrink, DennisBunse, CarinaLundin, DanielFarnelid, HannaLegrand, CatherinePinhassi, Jarone

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