From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management

Adina Zhumakhanova; Yersultan Mirasbekov; Ayagoz Meirkhanova; Dmitry V. Malashenkov; Thomas A. Davidson; Eti Ester Levi; Erik Jeppesen; Natasha S. Barteneva

doi:10.1016/j.ecolind.2024.112100

From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management

Adina Zhumakhanova, Yersultan Mirasbekov, Ayagoz Meirkhanova, Dmitry V. Malashenkov, Thomas A. Davidson, Eti Ester Levi, Erik Jeppesen, Natasha S. Barteneva^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

1 Citation (Scopus)

Abstract

The alarming increase in the frequency of blooms of Microcystis in freshwater lakes and reservoirs occurs worldwide, with major implications for their ecosystem functioning and water quality. The dominance of Microcystis is tightly related to colonial formation by Microcystis. However, studies of the colonial development of Microcystis morphospecies are rare. This research applied FlowCAM-based imaging flow cytometry to analyze the development of Microcystis morphospecies in the mesocosms mimicking eutrophic shallow lakes and the effect of temperature changes. A significant positive association was found between M. ichtyoblabe, M. aeruginosa, and M. smithii colonies, particularly in the high-temperature tanks, suggesting that these morphospecies belong to one ecocluster, which supports the hypothesis of the central transition pathways of colonial Microcystis. The small colonial clusters of Microcystis cells represented an important stage in the sequence of Microcystis bloom and were associated with the development of colonial forms. A correlation analysis showed that the higher pH was positively correlated with the abundance of M.wesenbergii independently of temperature changes. The colonial sheaths' abundances increased following a maximum of M.wesenbergii abundance, reaching significant numbers (thousands), and a majority of sheaths contained at least some Microcystis cells. We hypothesize that colonial sheaths may be crucial at Microcystis spp. dispersal and represent an obligatory stage of colonies development. The sheaths may protect Microcystis cells against environmental stress factors, improve cell survival at low nutrient levels, and participate in Microcystis dispersal and spreading. Our findings can be applicable to early CyanoHAB detection and management of Microcystis dispersal.

Original language	English
Article number	112100
Journal	Ecological Indicators
Volume	163
ISSN	1470-160X
DOIs	https://doi.org/10.1016/j.ecolind.2024.112100
Publication status	Published - Jun 2024

Keywords

Colonial clusters
Colonial sheaths
Cyanobacteria
Dispersal
FlowCAM
Imaging flow cytometry
Microcystis
Phytoplankton

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10.1016/j.ecolind.2024.112100

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Zhumakhanova, A., Mirasbekov, Y., Meirkhanova, A., Malashenkov, D. V., Davidson, T. A., Levi, E. E., Jeppesen, E., & Barteneva, N. S. (2024). From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management. Ecological Indicators, 163, Article 112100. https://doi.org/10.1016/j.ecolind.2024.112100

@article{57dff9e5990a41b68d2d7152ef82aa27,

title = "From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management",

abstract = "The alarming increase in the frequency of blooms of Microcystis in freshwater lakes and reservoirs occurs worldwide, with major implications for their ecosystem functioning and water quality. The dominance of Microcystis is tightly related to colonial formation by Microcystis. However, studies of the colonial development of Microcystis morphospecies are rare. This research applied FlowCAM-based imaging flow cytometry to analyze the development of Microcystis morphospecies in the mesocosms mimicking eutrophic shallow lakes and the effect of temperature changes. A significant positive association was found between M. ichtyoblabe, M. aeruginosa, and M. smithii colonies, particularly in the high-temperature tanks, suggesting that these morphospecies belong to one ecocluster, which supports the hypothesis of the central transition pathways of colonial Microcystis. The small colonial clusters of Microcystis cells represented an important stage in the sequence of Microcystis bloom and were associated with the development of colonial forms. A correlation analysis showed that the higher pH was positively correlated with the abundance of M.wesenbergii independently of temperature changes. The colonial sheaths' abundances increased following a maximum of M.wesenbergii abundance, reaching significant numbers (thousands), and a majority of sheaths contained at least some Microcystis cells. We hypothesize that colonial sheaths may be crucial at Microcystis spp. dispersal and represent an obligatory stage of colonies development. The sheaths may protect Microcystis cells against environmental stress factors, improve cell survival at low nutrient levels, and participate in Microcystis dispersal and spreading. Our findings can be applicable to early CyanoHAB detection and management of Microcystis dispersal.",

keywords = "Colonial clusters, Colonial sheaths, Cyanobacteria, Dispersal, FlowCAM, Imaging flow cytometry, Microcystis, Phytoplankton",

author = "Adina Zhumakhanova and Yersultan Mirasbekov and Ayagoz Meirkhanova and Malashenkov, {Dmitry V.} and Davidson, {Thomas A.} and Levi, {Eti Ester} and Erik Jeppesen and Barteneva, {Natasha S.}",

note = "Publisher Copyright: {\textcopyright} 2024",

year = "2024",

month = jun,

doi = "10.1016/j.ecolind.2024.112100",

language = "English",

volume = "163",

journal = "Ecological Indicators",

issn = "1470-160X",

publisher = "Elsevier B.V.",

}

Zhumakhanova, A, Mirasbekov, Y, Meirkhanova, A, Malashenkov, DV, Davidson, TA , Levi, EE , Jeppesen, E & Barteneva, NS 2024, 'From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management', Ecological Indicators, vol. 163, 112100. https://doi.org/10.1016/j.ecolind.2024.112100

From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management. / Zhumakhanova, Adina; Mirasbekov, Yersultan; Meirkhanova, Ayagoz et al.
In: Ecological Indicators, Vol. 163, 112100, 06.2024.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - From colonial clusters to colonial sheaths

T2 - Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management

AU - Zhumakhanova, Adina

AU - Mirasbekov, Yersultan

AU - Meirkhanova, Ayagoz

AU - Malashenkov, Dmitry V.

AU - Davidson, Thomas A.

AU - Levi, Eti Ester

AU - Jeppesen, Erik

AU - Barteneva, Natasha S.

PY - 2024/6

Y1 - 2024/6

N2 - The alarming increase in the frequency of blooms of Microcystis in freshwater lakes and reservoirs occurs worldwide, with major implications for their ecosystem functioning and water quality. The dominance of Microcystis is tightly related to colonial formation by Microcystis. However, studies of the colonial development of Microcystis morphospecies are rare. This research applied FlowCAM-based imaging flow cytometry to analyze the development of Microcystis morphospecies in the mesocosms mimicking eutrophic shallow lakes and the effect of temperature changes. A significant positive association was found between M. ichtyoblabe, M. aeruginosa, and M. smithii colonies, particularly in the high-temperature tanks, suggesting that these morphospecies belong to one ecocluster, which supports the hypothesis of the central transition pathways of colonial Microcystis. The small colonial clusters of Microcystis cells represented an important stage in the sequence of Microcystis bloom and were associated with the development of colonial forms. A correlation analysis showed that the higher pH was positively correlated with the abundance of M.wesenbergii independently of temperature changes. The colonial sheaths' abundances increased following a maximum of M.wesenbergii abundance, reaching significant numbers (thousands), and a majority of sheaths contained at least some Microcystis cells. We hypothesize that colonial sheaths may be crucial at Microcystis spp. dispersal and represent an obligatory stage of colonies development. The sheaths may protect Microcystis cells against environmental stress factors, improve cell survival at low nutrient levels, and participate in Microcystis dispersal and spreading. Our findings can be applicable to early CyanoHAB detection and management of Microcystis dispersal.

AB - The alarming increase in the frequency of blooms of Microcystis in freshwater lakes and reservoirs occurs worldwide, with major implications for their ecosystem functioning and water quality. The dominance of Microcystis is tightly related to colonial formation by Microcystis. However, studies of the colonial development of Microcystis morphospecies are rare. This research applied FlowCAM-based imaging flow cytometry to analyze the development of Microcystis morphospecies in the mesocosms mimicking eutrophic shallow lakes and the effect of temperature changes. A significant positive association was found between M. ichtyoblabe, M. aeruginosa, and M. smithii colonies, particularly in the high-temperature tanks, suggesting that these morphospecies belong to one ecocluster, which supports the hypothesis of the central transition pathways of colonial Microcystis. The small colonial clusters of Microcystis cells represented an important stage in the sequence of Microcystis bloom and were associated with the development of colonial forms. A correlation analysis showed that the higher pH was positively correlated with the abundance of M.wesenbergii independently of temperature changes. The colonial sheaths' abundances increased following a maximum of M.wesenbergii abundance, reaching significant numbers (thousands), and a majority of sheaths contained at least some Microcystis cells. We hypothesize that colonial sheaths may be crucial at Microcystis spp. dispersal and represent an obligatory stage of colonies development. The sheaths may protect Microcystis cells against environmental stress factors, improve cell survival at low nutrient levels, and participate in Microcystis dispersal and spreading. Our findings can be applicable to early CyanoHAB detection and management of Microcystis dispersal.

KW - Colonial clusters

KW - Colonial sheaths

KW - Cyanobacteria

KW - Dispersal

KW - FlowCAM

KW - Imaging flow cytometry

KW - Microcystis

KW - Phytoplankton

UR - http://www.scopus.com/inward/record.url?scp=85192298943&partnerID=8YFLogxK

U2 - 10.1016/j.ecolind.2024.112100

DO - 10.1016/j.ecolind.2024.112100

M3 - Journal article

AN - SCOPUS:85192298943

SN - 1470-160X

VL - 163

JO - Ecological Indicators

JF - Ecological Indicators

M1 - 112100

ER -

From colonial clusters to colonial sheaths: Imaging flow cytometry analysis of Microcystis morphospecies dynamics in mesocosm and links to CyanoHABs management

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