Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy

Abstract Background Technical limitations regarding bulk analysis of phytoplankton biomass limit our comprehension of carbon fluxes in natural populations and, therefore, of carbon, nutrients and energy cycling in aquatic ecosystems. In this study, we took advantage of Synchrotron FTIR micro-spectro...

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Main Authors: Andrea Fanesi, Heiko Wagner, Giovanni Birarda, Lisa Vaccari, Christian Wilhelm
Format: Article
Language:English
Published: BMC 2019-04-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-1736-8
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spelling doaj-77c3f9ab28f145afb70d7b928a0002362020-11-25T03:16:36ZengBMCBMC Plant Biology1471-22292019-04-0119111410.1186/s12870-019-1736-8Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopyAndrea Fanesi0Heiko Wagner1Giovanni Birarda2Lisa Vaccari3Christian Wilhelm4Department of Plant Physiology, Leipzig University, Institute of BiologyDepartment of Plant Physiology, Leipzig University, Institute of BiologyElettra - Sincrotrone Trieste, Synchrotron Infrared Source for Spectroscopy and Imaging – SISSIElettra - Sincrotrone Trieste, Synchrotron Infrared Source for Spectroscopy and Imaging – SISSIDepartment of Plant Physiology, Leipzig University, Institute of BiologyAbstract Background Technical limitations regarding bulk analysis of phytoplankton biomass limit our comprehension of carbon fluxes in natural populations and, therefore, of carbon, nutrients and energy cycling in aquatic ecosystems. In this study, we took advantage of Synchrotron FTIR micro-spectroscopy and the partial least square regression (PLSr) algorithm to simultaneously quantify the protein, lipid and carbohydrate content at the single-cell level in a mock phytoplankton community (composed by a cyanobacterium, a green-alga and a diatom) grown at two temperatures (15 °C and 25 °C). Results The PLSr models generated to quantify cell macromolecules presented high quality fit (R2 ≥ 0.90) and low error of prediction (RMSEP 2–6% of dry weight). The regression coefficients revealed that the prediction of each macromolecule was not exclusively dependent on spectral features corresponding to that compound, but rather on all major macromolecular pools, reflecting adjustments in the overall cell carbon balance. The single-cell analysis, studied by means of Kernel density estimators, showed that the modes of density distribution of macromolecules were different at 15 °C and 25 °C. However, a substantial proportion of cells was biochemically identical at the two temperatures because of population heterogeneity. Conclusions The spectroscopic approach presented in this study allows the quantification of macromolecules in single phytoplankton cells. This method showed that population heterogeneity most likely ensures a backup of non-acclimated cells that may rapidly exploit new favourable niches. This finding may have important consequences for the ecology of phytoplankton populations and shows that the “average cell” concept might substantially limit our comprehension of population dynamics and biogeochemical cycles in aquatic ecosystems.http://link.springer.com/article/10.1186/s12870-019-1736-8AlgaeChemometricsFTIR-spectroscopyMacromoleculesPhytoplanktonPLSr
collection DOAJ
language English
format Article
sources DOAJ
author Andrea Fanesi
Heiko Wagner
Giovanni Birarda
Lisa Vaccari
Christian Wilhelm
spellingShingle Andrea Fanesi
Heiko Wagner
Giovanni Birarda
Lisa Vaccari
Christian Wilhelm
Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
BMC Plant Biology
Algae
Chemometrics
FTIR-spectroscopy
Macromolecules
Phytoplankton
PLSr
author_facet Andrea Fanesi
Heiko Wagner
Giovanni Birarda
Lisa Vaccari
Christian Wilhelm
author_sort Andrea Fanesi
title Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
title_short Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
title_full Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
title_fullStr Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
title_full_unstemmed Quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell Synchrotron FTIR-spectroscopy
title_sort quantitative macromolecular patterns in phytoplankton communities resolved at the taxonomical level by single-cell synchrotron ftir-spectroscopy
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2019-04-01
description Abstract Background Technical limitations regarding bulk analysis of phytoplankton biomass limit our comprehension of carbon fluxes in natural populations and, therefore, of carbon, nutrients and energy cycling in aquatic ecosystems. In this study, we took advantage of Synchrotron FTIR micro-spectroscopy and the partial least square regression (PLSr) algorithm to simultaneously quantify the protein, lipid and carbohydrate content at the single-cell level in a mock phytoplankton community (composed by a cyanobacterium, a green-alga and a diatom) grown at two temperatures (15 °C and 25 °C). Results The PLSr models generated to quantify cell macromolecules presented high quality fit (R2 ≥ 0.90) and low error of prediction (RMSEP 2–6% of dry weight). The regression coefficients revealed that the prediction of each macromolecule was not exclusively dependent on spectral features corresponding to that compound, but rather on all major macromolecular pools, reflecting adjustments in the overall cell carbon balance. The single-cell analysis, studied by means of Kernel density estimators, showed that the modes of density distribution of macromolecules were different at 15 °C and 25 °C. However, a substantial proportion of cells was biochemically identical at the two temperatures because of population heterogeneity. Conclusions The spectroscopic approach presented in this study allows the quantification of macromolecules in single phytoplankton cells. This method showed that population heterogeneity most likely ensures a backup of non-acclimated cells that may rapidly exploit new favourable niches. This finding may have important consequences for the ecology of phytoplankton populations and shows that the “average cell” concept might substantially limit our comprehension of population dynamics and biogeochemical cycles in aquatic ecosystems.
topic Algae
Chemometrics
FTIR-spectroscopy
Macromolecules
Phytoplankton
PLSr
url http://link.springer.com/article/10.1186/s12870-019-1736-8
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