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Structuring of marine prokaryotic gene expression by temperature and dissolved organic matter
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.ORCID iD: 0000-0002-8779-6464
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Temperature and dissolved organic matter (DOM) are important drivers of marine microbial activity, but their effects, alone or in combination, on the physiological responses of sub-arctic prokaryotic assemblages remain poorly understood. In a one-month mesocosm experiment initiated in early March in the northern Baltic Sea, we thus exposed a coastal microbial community to temperature and nutrient regimes representative of winter and early summer (i.e., 1°C and 10°C, with and without DOM additions) in a 2x2 factorial design. Prokaryotic abundance and heterotrophic production increased until around day 17 in the 10°C mesocosms. Yet, mid through the experiment (days 10 and 17, when samples for metatranscriptomics analyses were analyzed), estimates of growth rates were highest for the 10°C plus DOM treatment (TN; ~2.5 day-1), comparable for the 1°C plus DOM (N) and the 10°C treatments (T; ~1.0 day-1), and low for the control (C; 0.2 day-1). PCA analysis showed that samples for prokaryotic transcription in the 1°C plus DOM and the 10°C treatments clustered in different directions from the control, and the combined 10°C plus DOM treatment triggered even further changes. Taxonomic analysis of the transcripts uncovered broad treatment specific responses. This included a dominance of Nitrosopumilus (Archaea) in the 1°C mesocosms (with and without DOM), an increase in the relative expression of Alphaproteobacteria (both Rhodobacterales and SAR11) in the 10°C mesocosms without DOM addition, and an increase in Oceanospirillales in the 10°C plus DOM treatment. Burkholderiales (Betaproteobacteria) maintained a high relative expression (up to 25%) in all mesocosms. A PERMANOVA on the total of 182,618 transcribed genes revealed statistically significant effects of both temperature and DOM, and also a significant interaction effect between the two factors. EdgeR analysis identified significant differential transcription for up to 10% of the genes in each of the tested contrasts. Prominent features among the significant genes included Nitrosopumilus genes for ammonium uptake and ammonia oxidation in the 1°C mesocosms (C, N), membrane transporters for small organic acids in the N-treatment, genes for N and P assimilation along with molecular chaperones in the T-treatment, and dominance of Oceanospirillales genes for energy and growth metabolism in the TN treatment. These metatranscriptomics responses were associated with changes in ecologically important characteristics of the prokaryotic communities, such as growth rates and growth efficiency, providing clues to how successional changes in community composition and metabolism are induced by environmental conditions linked with seasonality.

National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-129191OAI: oai:DiVA.org:lnu-129191DiVA, id: diva2:1856590
Available from: 2024-05-07 Created: 2024-05-07 Last updated: 2024-05-30
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)
Opponent
Supervisors
Available from: 2024-05-13 Created: 2024-05-07 Last updated: 2024-05-24Bibliographically approved

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Amnebrink, DennisLundin, DanielPinhassi, Jarone

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