Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture

ABSTRACT In this study, a strain of SAR11 subgroup IIIa (termed HIMB114) was grown in seawater-based batch and continuous culture in order to quantify cellular features and metabolism relevant to SAR11 ecology. We report some of the first direct measurements of cellular elemental quotas for nitrogen...

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Autores principales:	Scott R. Grant, Matthew J. Church, Sara Ferrón, Edward A. Laws, Michael S. Rappé
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	SAR11 bacterial production biogeochemistry marine microbiology phosphorous respiration Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/562a3651c3ec4069a392f73f723dd6ef
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spelling	oai:doaj.org-article:562a3651c3ec4069a392f73f723dd6ef2021-12-02T19:47:35ZElemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture10.1128/mSystems.00218-182379-5077https://doaj.org/article/562a3651c3ec4069a392f73f723dd6ef2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00218-18https://doaj.org/toc/2379-5077ABSTRACT In this study, a strain of SAR11 subgroup IIIa (termed HIMB114) was grown in seawater-based batch and continuous culture in order to quantify cellular features and metabolism relevant to SAR11 ecology. We report some of the first direct measurements of cellular elemental quotas for nitrogen (N) and phosphorus (P) for SAR11, grown in batch culture: 1.4 ± 0.9 fg N and 0.44 ± 0.01 fg P, respectively, that were consistent with the small size of HIMB114 cells (average volume of 0.09 μm3). However, the mean carbon (C) cellular quota of 50 ± 47 fg C was anomalously high, but variable. The rates of phosphate (PO43−) uptake measured from both batch and continuous cultures were exceptionally slow: in chemostats growing at 0.3 day−1, HIMB114 took up 1.1 ± 0.3 amol P cell−1 day−1, suggesting that <30% of the cellular P requirement of HIMB114 was met by PO43− assimilation. The mean rate of leucine incorporation, a measure of bacterial production, during late-log-phase growth of batch HIMB114 cultures was 0.042 ± 0.02 amol Leu cell−1 h−1. While only weakly correlated with changes in specific growth rates, the onset of stationary phase resulted in decreases in cell-specific leucine incorporation that were proportional to changes in growth rate. The rates of cellular production, respiratory oxygen consumption, and changes in total organic C concentrations constrained cellular growth efficiencies to 13% ± 4%. Hence, despite a small genome and diminutively sized cells, SAR11 strain HIMB114 appears to grow at efficiencies similar to those of naturally occurring bacterioplankton communities. IMPORTANCE While SAR11 bacteria contribute a significant fraction to the total picoplankton biomass in the ocean and likely are major players in organic C and nutrient cycling, the cellular characteristics and metabolic features of most lineages have either only been hypothesized from genomes or otherwise not measured in controlled laboratory experimentation. The dearth of data on even the most basic characteristics for what is arguably the most abundant heterotroph in seawater has limited the specific consideration of SAR11 in ocean ecosystem modeling efforts. In this study, we provide measures of cellular P, N, and C, aerobic respiration, and bacterial production for a SAR11 strain growing in natural seawater medium that can be used to directly relate these features of SAR11 to biogeochemical cycling in the oceans. Through the development of a chemostat system to measure nutrient uptake during steady-state growth, we have also documented inorganic P uptake rates that allude to the importance of organic phosphorous to meet cellular P demands, even in the presence of nonlimiting PO43− concentrations.Scott R. GrantMatthew J. ChurchSara FerrónEdward A. LawsMichael S. RappéAmerican Society for MicrobiologyarticleSAR11bacterial productionbiogeochemistrymarine microbiologyphosphorousrespirationMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	SAR11 bacterial production biogeochemistry marine microbiology phosphorous respiration Microbiology QR1-502
spellingShingle	SAR11 bacterial production biogeochemistry marine microbiology phosphorous respiration Microbiology QR1-502 Scott R. Grant Matthew J. Church Sara Ferrón Edward A. Laws Michael S. Rappé Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
description	ABSTRACT In this study, a strain of SAR11 subgroup IIIa (termed HIMB114) was grown in seawater-based batch and continuous culture in order to quantify cellular features and metabolism relevant to SAR11 ecology. We report some of the first direct measurements of cellular elemental quotas for nitrogen (N) and phosphorus (P) for SAR11, grown in batch culture: 1.4 ± 0.9 fg N and 0.44 ± 0.01 fg P, respectively, that were consistent with the small size of HIMB114 cells (average volume of 0.09 μm3). However, the mean carbon (C) cellular quota of 50 ± 47 fg C was anomalously high, but variable. The rates of phosphate (PO43−) uptake measured from both batch and continuous cultures were exceptionally slow: in chemostats growing at 0.3 day−1, HIMB114 took up 1.1 ± 0.3 amol P cell−1 day−1, suggesting that <30% of the cellular P requirement of HIMB114 was met by PO43− assimilation. The mean rate of leucine incorporation, a measure of bacterial production, during late-log-phase growth of batch HIMB114 cultures was 0.042 ± 0.02 amol Leu cell−1 h−1. While only weakly correlated with changes in specific growth rates, the onset of stationary phase resulted in decreases in cell-specific leucine incorporation that were proportional to changes in growth rate. The rates of cellular production, respiratory oxygen consumption, and changes in total organic C concentrations constrained cellular growth efficiencies to 13% ± 4%. Hence, despite a small genome and diminutively sized cells, SAR11 strain HIMB114 appears to grow at efficiencies similar to those of naturally occurring bacterioplankton communities. IMPORTANCE While SAR11 bacteria contribute a significant fraction to the total picoplankton biomass in the ocean and likely are major players in organic C and nutrient cycling, the cellular characteristics and metabolic features of most lineages have either only been hypothesized from genomes or otherwise not measured in controlled laboratory experimentation. The dearth of data on even the most basic characteristics for what is arguably the most abundant heterotroph in seawater has limited the specific consideration of SAR11 in ocean ecosystem modeling efforts. In this study, we provide measures of cellular P, N, and C, aerobic respiration, and bacterial production for a SAR11 strain growing in natural seawater medium that can be used to directly relate these features of SAR11 to biogeochemical cycling in the oceans. Through the development of a chemostat system to measure nutrient uptake during steady-state growth, we have also documented inorganic P uptake rates that allude to the importance of organic phosphorous to meet cellular P demands, even in the presence of nonlimiting PO43− concentrations.
format	article
author	Scott R. Grant Matthew J. Church Sara Ferrón Edward A. Laws Michael S. Rappé
author_facet	Scott R. Grant Matthew J. Church Sara Ferrón Edward A. Laws Michael S. Rappé
author_sort	Scott R. Grant
title	Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
title_short	Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
title_full	Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
title_fullStr	Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
title_full_unstemmed	Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture
title_sort	elemental composition, phosphorous uptake, and characteristics of growth of a sar11 strain in batch and continuous culture
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/562a3651c3ec4069a392f73f723dd6ef
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Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture

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