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Seasonal dynamics and life cycle strategies of the cyanobacterium Aphanizomenon in the Baltic proper
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
GEOMAR Helmholtz Centre ofr Ocean Research Kiel, Germany.ORCID iD: 0000-0003-4787-7021
University of La Laguna, Spain.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0002-8779-6464
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Aphanizomenon, together with Dolichospermum and Nodularia, constitute the major genera of bloom forming filamentous nitrogen fixing cyanobacteria in the Baltic Sea. Like the other genera, Aphanizomenon displays summer blooms that are highly variable in magnitude and duration but unlike the others it is considered a holoplanktonic species. Still, the molecular mechanisms enabling Aphanizomenon year-round presence in surface waters are currently unknown. Here we combine analysis of Aphanizomenon population dynamics at the Linnaeus Microbial Observatory (LMO) station in the Baltic Proper over nine years (2011-2019) with associated gene expression patterns during 2016-2017 to identify annual abundance, and metabolic and life cycle strategies. Aphanizomenon biomass showed large annual variability and a consistent biovolume peak in summer, with bloom intensity ranging from 78-1334 mm3 m-3. 16S rRNA gene amplicon sequence data showed that one Aphanizomenon amplicon sequence variant (ASV) dominated, and its relative abundance correlated with biovolume measurements. Metatranscriptomic reads that mapped to an Aphanizomenon metagenome- assembled genome (MAG) revealed annually repeating gene expression patterns, resulting in distinct gene expression profiles during different meteorological seasons. Genes encoding proteins involved in several important functional classes, e.g. carbon fixation, photosynthesis, and associated photopigments showed seasonal variation, but were detected year round. Other genes, particularly those involved in nitrogen fixation, were highly expressed in summer, while absent in winter. Vitamin metabolism and phosphorus scavenging genes were preferentially expressed during the colder periods of the annual cycle. Together, these data show that Aphanizomenon regulates the molecular machinery on the seasonal scale, providing context to the observed dynamics of Aphanizomenon in the Baltic Proper and a foundation for understanding the ecology of these cyanobacteria. 

National Category
Ecology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-129189OAI: oai:DiVA.org:lnu-129189DiVA, id: diva2:1856584
Available from: 2024-05-07 Created: 2024-05-07 Last updated: 2024-08-22Bibliographically 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: 2025-03-19Bibliographically approved

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Amnebrink, DennisPontiller, BenjaminLundin, DanielLegrand, CatherineLindehoff, ElinFarnelid, HannaPinhassi, Jarone

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