The phyto-bacterioplankton couple in a shallow freshwater ecosystem: Who leads the dance?

Louati, Imen; Nunan, Naoise; Tambosco, Kevin; Bernard, Cécile; Humbert, Jean‐François; Leloup, Julie

doi:10.1016/j.hal.2023.102436

Cited by 6 publications

(12 citation statements)

References 73 publications

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“…One of these features is the high and stable chlorophyll a concentration over time (mean concentrations ranging from 566 to 702 μg.L −1 , reported over the 2010–2015 period (Leboulanger et al., 2017), 587 μg.L −1 in 2018), which is of great interest in the study of phytoplanktonic phycosphere compared with other ecosystems where phytoplanktonic blooms occurs only periodically. In temperate areas where cyanobacterial blooms occur in lakes, they only appear during the summer period (Louati et al., 2023). Indeed, whatever the season, the cyanobacterium Arthrospira fusiformis and the picoeukaryotic algae Picocystis salinarum dominate the phototrophic microbial assemblage (Bernard et al., 2019) in the two main contrasted ecological niches of the water column: the photic upper layer (i.e.…”

Section: Introductionmentioning

confidence: 99%

Phytoplanktonic species in the haloalkaline Lake Dziani Dzaha select their archaeal microbiome

Bruto,

Oger,

Got

et al. 2023

Molecular Ecology

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Microorganisms are key contributors of aquatic biogeochemical cycles but their microscale ecology remains largely unexplored, especially interactions occurring between phytoplankton and microorganisms in the phycosphere, that is the region immediately surrounding phytoplankton cells. The current study aimed to provide evidence of the phycosphere taking advantage of a unique hypersaline, hyperalkaline ecosystem, Lake Dziani Dzaha (Mayotte), where two phytoplanktonic species permanently co‐dominate: a cyanobacterium, Arthrospira fusiformis, and a green microalga, Picocystis salinarum. To assay phycospheric microbial diversity from in situ sampling, we set up a flow cytometry cell‐sorting methodology for both phytoplanktonic populations, coupled with metabarcoding and comparative microbiome diversity. We focused on archaeal communities as they represent a non‐negligible part of the phycospheric diversity, however their role is poorly understood. This work is the first which successfully explores in situ archaeal diversity distribution showing contrasted phycospheric compositions, with P. salinarum phycosphere notably enriched in Woesearchaeales OTUs while A. fusiformis phycosphere was enriched in methanogenic lineages affiliated OTUs such as Methanomicrobiales or Methanofastidiosales. Most archaeal OTUs, including Woesearchaeales considered in literature as symbionts, were either ubiquitous or specific of the free‐living microbiome (i.e. present in the 3–0.2 μm fraction). Seminally, several archaeal OTUs were enriched from the free‐living microbiome to the phytoplankton phycospheres, suggesting (i) either the inhibition or decrease of other OTUs, or (ii) the selection of specific OTUs resulting from the physical influence of phytoplanktonic species on surrounding Archaea.

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Section: Introductionmentioning

confidence: 99%

Phytoplanktonic species in the haloalkaline Lake Dziani Dzaha select their archaeal microbiome

Bruto,

Oger,

Got

et al. 2023

Molecular Ecology

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“…Relationships between Microcystis and bacteria have been the focus of much research (e.g., Cook et al, 2020 ; Smith et al, 2022 ). However, these studies have concentrated on the relationships between Microcystis and the epibiont bacterial communities (e.g., Cook et al, 2020 ; Smith et al, 2021 ) or understanding the distinctions between epibiont and pelagic bacterial communities during bloom conditions (e.g., Parveen et al, 2013 ; Louati et al, 2023 ). However, temporal associations between cyanobacterial and co-occurring bacterioplankton during non-bloom conditions are rarely investigated.…”

Section: Discussionmentioning

confidence: 99%

“…Despite their close relationships, the role of bacteria in cyanoHABs and relationships with bloom-forming cyanobacteria are often overlooked ( Pound et al, 2021 ). Furthermore, the majority of the focus on bacterial-cyanobacterial interactions have centered on the phycosphere (i.e., epibionts or particle-associated) bacteria, with less focus on the bacterioplankton (i.e., free-living; Louati et al, 2023 ).…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal diversity and community structure of cyanobacteria and associated bacteria in the large shallow subtropical Lake Okeechobee (Florida, United States)

Lefler,

Barbosa,

Zimba

et al. 2023

Front. Microbiol.

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Lake Okeechobee is a large eutrophic, shallow, subtropical lake in south Florida, United States. Due to decades of nutrient loading and phosphorus rich sediments, the lake is eutrophic and frequently experiences cyanobacterial harmful algal blooms (cyanoHABs). In the past, surveys of the phytoplankton community structure in the lake have been conducted by morphological studies, whereas molecular based studies have been seldom employed. With increased frequency of cyanoHABs in Lake Okeechobee (e.g., 2016 and 2018 Microcystis-dominated blooms), it is imperative to determine the diversity of cyanobacterial taxa that exist within the lake and the limnological parameters that drive bloom-forming genera. A spatiotemporal study of the lake was conducted over the course of 1 year to characterize the (cyano)bacterial community structure, using 16S rRNA metabarcoding, with coincident collection of limnological parameters (e.g., nutrients, water temperature, major ions), and cyanotoxins. The objectives of this study were to elucidate spatiotemporal trends of community structure, identify drivers of community structure, and examine cyanobacteria-bacterial relationships within the lake. Results indicated that cyanobacterial communities within the lake were significantly different between the wet and dry season, but not between periods of nitrogen limitation and co-nutrient limitation. Throughout the year, the lake was primarily dominated by the picocyanobacterium Cyanobium. The bloom-forming genera Cuspidothrix, Dolichospermum, Microcystis, and Raphidiopsis were highly abundant throughout the lake and had disparate nutrient requirements and niches within the lake. Anatoxin-a, microcystins, and nodularins were detected throughout the lake across both seasons. There were no correlated (cyano)bacteria shared between the common bloom-forming cyanobacteria Dolichospermum, Microcystis, and Raphidiopsis. This study is the first of its kind to use molecular based methods to assess the cyanobacterial community structure within the lake. These data greatly improve our understanding of the cyanobacterial community structure within the lake and the physiochemical parameters which may drive the bloom-forming taxa within Lake Okeechobee.

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“…It is worth noting that not all coexisting plankton species necessarily engage in direct competition with cyanobacteria. Some bacterioplankton species have specialized ecological niches or utilize different resources, enabling coexistence without direct competition . Investigating the functional potential of co-occurring bacterioplankton is an urgent need to better understand the ecology of toxin producers concerning N and P concentrations during a bloom period, e.g., from start to end .…”

Section: Introductionmentioning

confidence: 99%

“…Investigating the functional potential of co-occurring bacterioplankton is an urgent need to better understand the ecology of toxin producers concerning N and P concentrations during a bloom period, e.g., from start to end . Previous but limited efforts have revealed specific bacterial taxa that are commonly found during bloom and their ecological functions, such as the release of organic compounds. ,, However, our understanding of the role and dynamics of other bacterioplankton species during cyanoHABs is still limited . Cyanobacteria and bacterioplankton have developed distinct strategies to adapt to nutrient deprivation and environmental stress.…”

Section: Introductionmentioning

confidence: 99%

Stringent Response of Cyanobacteria and Other Bacterioplankton during Different Stages of a Harmful Cyanobacterial Bloom

Li,

Bhattarai,

Barber

et al. 2023

Environ. Sci. Technol.

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We conducted a field study to investigate the role of stringent response in cyanobacteria and coexisting bacterioplankton during nutrient-deprived periods at various stages of bloom in a freshwater lake (Utah Lake) for the first time. Using metagenomics and metatranscriptomics analyses, we examined the cyanobacterial ecology and expression of important functional genes related to stringent response, N and P metabolism, and regulation. Our findings mark a significant advancement in understanding the mechanisms by which toxic cyanobacteria survive and proliferate during nitrogen (N) and phosphorus (P) limitations. We successfully identified and analyzed the metagenome-assembled genomes (MAGs) of the dominant bloom-forming cyanobacteria, namely, Dolichospermum circinale, Aphanizomenon flos-aquae UKL13-PB, Planktothrix agardhii, and Microcystis aeruginosa. By mapping RNA-seq data to the coding sequences of the MAGs, we observed that these four prevalent cyanobacteria species activated multiple functions to adapt to the depletion of inorganic nutrients. During and after the blooms, the four dominant cyanobacteria species expressed high levels of transcripts related to toxin production, such as microcystins (mcy), anatoxins (ana), and cylindrospermopsins (cyr). Additionally, genes associated with polyphosphate (poly-P) storage and the stringent response alarmone (p)ppGpp synthesis/hydrolysis, including ppk, relA, and spoT, were highly activated in both cyanobacteria and bacterioplankton. Under N deficiency, the main N pathways shifted from denitrification and dissimilatory nitrate reduction in bacterioplankton toward N2-fixing and assimilatory nitrate reduction in certain cyanobacteria with a corresponding shift in the community composition. P deprivation triggered a stringent response mediated by spoT-dependent (p)ppGpp accumulation and activation of the Pho regulon in both cyanobacteria and bacterioplankton, facilitating inorganic and organic P uptake. The dominant cyanobacterial MAGs exhibited the presence of multiple alkaline phosphatase (APase) transcripts (e.g., phoA in Dolichospermum, phoX in Planktothrix, and Microcystis), suggesting their ability to synthesize and release APase enzymes to convert ambient organic P into bioavailable forms. Conversely, transcripts associated with bacterioplankton-dominated pathways like denitrification were low and did not align with the occurrence of intense cyanoHABs. The strong correlations observed among N, P, stringent response metabolisms and the succession of blooms caused by dominant cyanobacterial species provide evidence that the stringent response, induced by nutrient limitation, may activate unique N and P functions in toxin-producing cyanobacteria, thereby sustaining cyanoHABs.

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The phyto-bacterioplankton couple in a shallow freshwater ecosystem: Who leads the dance?

Cited by 6 publications

References 73 publications

Phytoplanktonic species in the haloalkaline Lake Dziani Dzaha select their archaeal microbiome

Phytoplanktonic species in the haloalkaline Lake Dziani Dzaha select their archaeal microbiome

Spatiotemporal diversity and community structure of cyanobacteria and associated bacteria in the large shallow subtropical Lake Okeechobee (Florida, United States)

Stringent Response of Cyanobacteria and Other Bacterioplankton during Different Stages of a Harmful Cyanobacterial Bloom

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