Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm

ABSTRACT Although it is becoming clear that many microbial primary producers can also play a role as organic consumers, we know very little about the metabolic regulation of photoautotroph organic matter consumption. Cyanobacteria in phototrophic biofilms can reuse extracellular organic carbon, but...

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Autores principales:	Rhona K. Stuart, Xavier Mayali, Amy A. Boaro, Adam Zemla, R. Craig Everroad, Daniel Nilson, Peter K. Weber, Mary Lipton, Brad M. Bebout, Jennifer Pett-Ridge, Michael P. Thelen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/655fee623a3f4d199ab88db0e72a9600
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spelling	oai:doaj.org-article:655fee623a3f4d199ab88db0e72a96002021-11-15T15:50:17ZLight Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm10.1128/mBio.00650-162150-7511https://doaj.org/article/655fee623a3f4d199ab88db0e72a96002016-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00650-16https://doaj.org/toc/2150-7511ABSTRACT Although it is becoming clear that many microbial primary producers can also play a role as organic consumers, we know very little about the metabolic regulation of photoautotroph organic matter consumption. Cyanobacteria in phototrophic biofilms can reuse extracellular organic carbon, but the metabolic drivers of extracellular processes are surprisingly complex. We investigated the metabolic foundations of organic matter reuse by comparing exoproteome composition and incorporation of 13C-labeled and 15N-labeled cyanobacterial extracellular organic matter (EOM) in a unicyanobacterial biofilm incubated using different light regimes. In the light and the dark, cyanobacterial direct organic C assimilation accounted for 32% and 43%, respectively, of all organic C assimilation in the community. Under photosynthesis conditions, we measured increased excretion of extracellular polymeric substances (EPS) and proteins involved in micronutrient transport, suggesting that requirements for micronutrients may drive EOM assimilation during daylight hours. This interpretation was supported by photosynthesis inhibition experiments, in which cyanobacteria incorporated N-rich EOM-derived material. In contrast, under dark, C-starved conditions, cyanobacteria incorporated C-rich EOM-derived organic matter, decreased excretion of EPS, and showed an increased abundance of degradative exoproteins, demonstrating the use of the extracellular domain for C storage. Sequence-structure modeling of one of these exoproteins predicted a specific hydrolytic activity that was subsequently detected, confirming increased EOM degradation in the dark. Associated heterotrophic bacteria increased in abundance and upregulated transport proteins under dark relative to light conditions. Taken together, our results indicate that biofilm cyanobacteria are successful competitors for organic C and N and that cyanobacterial nutrient and energy requirements control the use of EOM. IMPORTANCE Cyanobacteria are globally distributed primary producers, and the fate of their fixed C influences microbial biogeochemical cycling. This fate is complicated by cyanobacterial degradation and assimilation of organic matter, but because cyanobacteria are assumed to be poor competitors for organic matter consumption, regulation of this process is not well tested. In mats and biofilms, this is especially relevant because cyanobacteria produce an extensive organic extracellular matrix, providing the community with a rich source of nutrients. Light is a well-known regulator of cyanobacterial metabolism, so we characterized the effects of light availability on the incorporation of organic matter. Using stable isotope tracing at the single-cell level, we quantified photoautotroph assimilation under different metabolic conditions and integrated the results with proteomics to elucidate metabolic status. We found that cyanobacteria effectively compete for organic matter in the light and the dark and that nutrient requirements and community interactions contribute to cycling of extracellular organic matter.Rhona K. StuartXavier MayaliAmy A. BoaroAdam ZemlaR. Craig EverroadDaniel NilsonPeter K. WeberMary LiptonBrad M. BeboutJennifer Pett-RidgeMichael P. ThelenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Rhona K. Stuart Xavier Mayali Amy A. Boaro Adam Zemla R. Craig Everroad Daniel Nilson Peter K. Weber Mary Lipton Brad M. Bebout Jennifer Pett-Ridge Michael P. Thelen Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
description	ABSTRACT Although it is becoming clear that many microbial primary producers can also play a role as organic consumers, we know very little about the metabolic regulation of photoautotroph organic matter consumption. Cyanobacteria in phototrophic biofilms can reuse extracellular organic carbon, but the metabolic drivers of extracellular processes are surprisingly complex. We investigated the metabolic foundations of organic matter reuse by comparing exoproteome composition and incorporation of 13C-labeled and 15N-labeled cyanobacterial extracellular organic matter (EOM) in a unicyanobacterial biofilm incubated using different light regimes. In the light and the dark, cyanobacterial direct organic C assimilation accounted for 32% and 43%, respectively, of all organic C assimilation in the community. Under photosynthesis conditions, we measured increased excretion of extracellular polymeric substances (EPS) and proteins involved in micronutrient transport, suggesting that requirements for micronutrients may drive EOM assimilation during daylight hours. This interpretation was supported by photosynthesis inhibition experiments, in which cyanobacteria incorporated N-rich EOM-derived material. In contrast, under dark, C-starved conditions, cyanobacteria incorporated C-rich EOM-derived organic matter, decreased excretion of EPS, and showed an increased abundance of degradative exoproteins, demonstrating the use of the extracellular domain for C storage. Sequence-structure modeling of one of these exoproteins predicted a specific hydrolytic activity that was subsequently detected, confirming increased EOM degradation in the dark. Associated heterotrophic bacteria increased in abundance and upregulated transport proteins under dark relative to light conditions. Taken together, our results indicate that biofilm cyanobacteria are successful competitors for organic C and N and that cyanobacterial nutrient and energy requirements control the use of EOM. IMPORTANCE Cyanobacteria are globally distributed primary producers, and the fate of their fixed C influences microbial biogeochemical cycling. This fate is complicated by cyanobacterial degradation and assimilation of organic matter, but because cyanobacteria are assumed to be poor competitors for organic matter consumption, regulation of this process is not well tested. In mats and biofilms, this is especially relevant because cyanobacteria produce an extensive organic extracellular matrix, providing the community with a rich source of nutrients. Light is a well-known regulator of cyanobacterial metabolism, so we characterized the effects of light availability on the incorporation of organic matter. Using stable isotope tracing at the single-cell level, we quantified photoautotroph assimilation under different metabolic conditions and integrated the results with proteomics to elucidate metabolic status. We found that cyanobacteria effectively compete for organic matter in the light and the dark and that nutrient requirements and community interactions contribute to cycling of extracellular organic matter.
format	article
author	Rhona K. Stuart Xavier Mayali Amy A. Boaro Adam Zemla R. Craig Everroad Daniel Nilson Peter K. Weber Mary Lipton Brad M. Bebout Jennifer Pett-Ridge Michael P. Thelen
author_facet	Rhona K. Stuart Xavier Mayali Amy A. Boaro Adam Zemla R. Craig Everroad Daniel Nilson Peter K. Weber Mary Lipton Brad M. Bebout Jennifer Pett-Ridge Michael P. Thelen
author_sort	Rhona K. Stuart
title	Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
title_short	Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
title_full	Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
title_fullStr	Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
title_full_unstemmed	Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm
title_sort	light regimes shape utilization of extracellular organic c and n in a cyanobacterial biofilm
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/655fee623a3f4d199ab88db0e72a9600
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Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm

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