Metabolic history and metabolic fitness as drivers of anabolic heterogeneity in isogenic microbial populations

Summary Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrien...

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Published in:	Environmental microbiology Vol. 23; no. 11; pp. 6764 - 6776
Main Authors:	Calabrese, Federica, Stryhanyuk, Hryhoriy, Moraru, Cristina, Schlömann, Michael, Wick, Lukas Y., Richnow, Hans H., Musat, Florin, Musat, Niculina
Format:	Journal Article
Language:	English
Published:	Hoboken, USA John Wiley & Sons, Inc 01.11.2021 Wiley Subscription Services, Inc
Subjects:	Acetates Acetic acid Anabolism Assimilation Benzoates Benzoic acid Fitness Heterogeneity Isotopes Mass spectrometry Mass spectroscopy Metabolic Networks and Pathways Metabolic pathways Metabolism microbiology Microorganisms Mineral nutrients Nutrient dynamics Populations Pseudomonas putida Pseudomonas putida - genetics Secondary ion mass spectrometry Spectrometry, Mass, Secondary Ion Stable isotopes Substrates Thauera aromatica Trends
ISSN:	1462-2912, 1462-2920, 1462-2920
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Abstract	Summary Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrient replete conditions. We applied time‐resolved stable isotope probing and nanoscale secondary ion mass spectrometry to quantify substrate assimilation by individual cells of Pseudomonas putida, P. stutzeri and Thauera aromatica. Acetate and benzoate at different concentrations were used as substrates. Anabolic heterogeneity was quantified by the cumulative differentiation tendency index. We observed two major, opposing trends of anabolic heterogeneity over time. Most often, microbial populations started as highly heterogeneous, with heterogeneity decreasing by various degrees over time. The second, less frequently observed trend, saw microbial populations starting at low or very low heterogeneity, and remaining largely stable over time. We explain these trends as an interplay of metabolic history (e.g. former growth substrate or other nutrient limitations) and metabolic fitness (i.e. the fine‐tuning of metabolic pathways to process a defined growth substrate). Our results offer a new viewpoint on the intra‐population functional diversification often encountered in the environment, and suggests that some microbial populations may be intrinsically heterogeneous.
AbstractList	Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrient replete conditions. We applied time‐resolved stable isotope probing and nanoscale secondary ion mass spectrometry to quantify substrate assimilation by individual cells of Pseudomonas putida, P. stutzeri and Thauera aromatica. Acetate and benzoate at different concentrations were used as substrates. Anabolic heterogeneity was quantified by the cumulative differentiation tendency index. We observed two major, opposing trends of anabolic heterogeneity over time. Most often, microbial populations started as highly heterogeneous, with heterogeneity decreasing by various degrees over time. The second, less frequently observed trend, saw microbial populations starting at low or very low heterogeneity, and remaining largely stable over time. We explain these trends as an interplay of metabolic history (e.g. former growth substrate or other nutrient limitations) and metabolic fitness (i.e. the fine‐tuning of metabolic pathways to process a defined growth substrate). Our results offer a new viewpoint on the intra‐population functional diversification often encountered in the environment, and suggests that some microbial populations may be intrinsically heterogeneous. Summary Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrient replete conditions. We applied time‐resolved stable isotope probing and nanoscale secondary ion mass spectrometry to quantify substrate assimilation by individual cells of Pseudomonas putida, P. stutzeri and Thauera aromatica. Acetate and benzoate at different concentrations were used as substrates. Anabolic heterogeneity was quantified by the cumulative differentiation tendency index. We observed two major, opposing trends of anabolic heterogeneity over time. Most often, microbial populations started as highly heterogeneous, with heterogeneity decreasing by various degrees over time. The second, less frequently observed trend, saw microbial populations starting at low or very low heterogeneity, and remaining largely stable over time. We explain these trends as an interplay of metabolic history (e.g. former growth substrate or other nutrient limitations) and metabolic fitness (i.e. the fine‐tuning of metabolic pathways to process a defined growth substrate). Our results offer a new viewpoint on the intra‐population functional diversification often encountered in the environment, and suggests that some microbial populations may be intrinsically heterogeneous. Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrient replete conditions. We applied time-resolved stable isotope probing and nanoscale secondary ion mass spectrometry to quantify substrate assimilation by individual cells of Pseudomonas putida, P. stutzeri and Thauera aromatica. Acetate and benzoate at different concentrations were used as substrates. Anabolic heterogeneity was quantified by the cumulative differentiation tendency index. We observed two major, opposing trends of anabolic heterogeneity over time. Most often, microbial populations started as highly heterogeneous, with heterogeneity decreasing by various degrees over time. The second, less frequently observed trend, saw microbial populations starting at low or very low heterogeneity, and remaining largely stable over time. We explain these trends as an interplay of metabolic history (e.g. former growth substrate or other nutrient limitations) and metabolic fitness (i.e. the fine-tuning of metabolic pathways to process a defined growth substrate). Our results offer a new viewpoint on the intra-population functional diversification often encountered in the environment, and suggests that some microbial populations may be intrinsically heterogeneous.Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that nutrient limitations are a relevant trigger for this behaviour. Here we explore the dynamics of anabolic heterogeneity under nutrient replete conditions. We applied time-resolved stable isotope probing and nanoscale secondary ion mass spectrometry to quantify substrate assimilation by individual cells of Pseudomonas putida, P. stutzeri and Thauera aromatica. Acetate and benzoate at different concentrations were used as substrates. Anabolic heterogeneity was quantified by the cumulative differentiation tendency index. We observed two major, opposing trends of anabolic heterogeneity over time. Most often, microbial populations started as highly heterogeneous, with heterogeneity decreasing by various degrees over time. The second, less frequently observed trend, saw microbial populations starting at low or very low heterogeneity, and remaining largely stable over time. We explain these trends as an interplay of metabolic history (e.g. former growth substrate or other nutrient limitations) and metabolic fitness (i.e. the fine-tuning of metabolic pathways to process a defined growth substrate). Our results offer a new viewpoint on the intra-population functional diversification often encountered in the environment, and suggests that some microbial populations may be intrinsically heterogeneous.
Author	Musat, Florin Richnow, Hans H. Stryhanyuk, Hryhoriy Wick, Lukas Y. Schlömann, Michael Calabrese, Federica Musat, Niculina Moraru, Cristina
Author_xml	– sequence: 1 givenname: Federica surname: Calabrese fullname: Calabrese, Federica organization: Helmholtz Centre for Environmental Research‐UFZ – sequence: 2 givenname: Hryhoriy surname: Stryhanyuk fullname: Stryhanyuk, Hryhoriy organization: Helmholtz Centre for Environmental Research‐UFZ – sequence: 3 givenname: Cristina surname: Moraru fullname: Moraru, Cristina organization: Carl von Ossietzky University of Oldenburg – sequence: 4 givenname: Michael surname: Schlömann fullname: Schlömann, Michael organization: Institute of Biosciences – sequence: 5 givenname: Lukas Y. surname: Wick fullname: Wick, Lukas Y. organization: Helmholtz Centre for Environmental Research‐UFZ – sequence: 6 givenname: Hans H. surname: Richnow fullname: Richnow, Hans H. organization: Helmholtz Centre for Environmental Research‐UFZ – sequence: 7 givenname: Florin orcidid: 0000-0002-4240-3495 surname: Musat fullname: Musat, Florin organization: Helmholtz Centre for Environmental Research‐UFZ – sequence: 8 givenname: Niculina orcidid: 0000-0001-9539-189X surname: Musat fullname: Musat, Niculina email: niculina.musat@ufz.de organization: Helmholtz Centre for Environmental Research‐UFZ
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Snippet	Summary Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been... Microbial populations often display different degrees of heterogeneity in their substrate assimilation, that is, anabolic heterogeneity. It has been shown that...
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SubjectTerms	Acetates Acetic acid Anabolism Assimilation Benzoates Benzoic acid Fitness Heterogeneity Isotopes Mass spectrometry Mass spectroscopy Metabolic Networks and Pathways Metabolic pathways Metabolism microbiology Microorganisms Mineral nutrients Nutrient dynamics Populations Pseudomonas putida Pseudomonas putida - genetics Secondary ion mass spectrometry Spectrometry, Mass, Secondary Ion Stable isotopes Substrates Thauera aromatica Trends
Title	Metabolic history and metabolic fitness as drivers of anabolic heterogeneity in isogenic microbial populations
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