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Prokaryotic maintenance respiration and growth efficiency field patterns reproduced by temperature and nutrient control at mesocosm scale
Umeå University, Sweden.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0002-2747-6346
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Linnaeus University, Linnaeus Knowledge Environments, Water. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0002-6405-1347
Umeå University, Sweden.
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. Vol. 25, no 3, p. 721-737
National Category
Ecology Microbiology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-118752DOI: 10.1111/1462-2920.16300ISI: 000905378800001PubMedID: 36511634Scopus ID: 2-s2.0-85145287538OAI: oai:DiVA.org:lnu-118752DiVA, id: diva2:1731317
Available from: 2023-01-26 Created: 2023-01-26 Last updated: 2024-05-07Bibliographically approved
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, DennisPinhassi, Jarone

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