Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

ABSTRACT Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown,...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Kasia Piwosz, Ana Vrdoljak, Thijs Frenken, Juan Manuel González-Olalla, Danijela Šantić, R. Michael McKay, Kristian Spilling, Lior Guttman, Petr Znachor, Izabela Mujakić, Lívia Kolesár Fecskeová, Luca Zoccarato, Martina Hanusová, Andrea Pessina, Tom Reich, Hans-Peter Grossart, Michal Koblížek
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	phytoplankton-bacteria coupling aerobic anoxygenic phototrophic bacteria bacterial community composition AAP community composition Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0144a2c1fc7c4410923a2f33b43d40f3
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:0144a2c1fc7c4410923a2f33b43d40f3
record_format	dspace
spelling	oai:doaj.org-article:0144a2c1fc7c4410923a2f33b43d40f32021-11-15T15:30:51ZLight and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment10.1128/mSphere.00354-202379-5042https://doaj.org/article/0144a2c1fc7c4410923a2f33b43d40f32020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00354-20https://doaj.org/toc/2379-5042ABSTRACT Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions. IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.Kasia PiwoszAna VrdoljakThijs FrenkenJuan Manuel González-OlallaDanijela ŠantićR. Michael McKayKristian SpillingLior GuttmanPetr ZnachorIzabela MujakićLívia Kolesár FecskeováLuca ZoccaratoMartina HanusováAndrea PessinaTom ReichHans-Peter GrossartMichal KoblížekAmerican Society for Microbiologyarticlephytoplankton-bacteria couplingaerobic anoxygenic phototrophic bacteriabacterial community compositionAAP community compositionMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	phytoplankton-bacteria coupling aerobic anoxygenic phototrophic bacteria bacterial community composition AAP community composition Microbiology QR1-502
spellingShingle	phytoplankton-bacteria coupling aerobic anoxygenic phototrophic bacteria bacterial community composition AAP community composition Microbiology QR1-502 Kasia Piwosz Ana Vrdoljak Thijs Frenken Juan Manuel González-Olalla Danijela Šantić R. Michael McKay Kristian Spilling Lior Guttman Petr Znachor Izabela Mujakić Lívia Kolesár Fecskeová Luca Zoccarato Martina Hanusová Andrea Pessina Tom Reich Hans-Peter Grossart Michal Koblížek Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
description	ABSTRACT Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions. IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.
format	article
author	Kasia Piwosz Ana Vrdoljak Thijs Frenken Juan Manuel González-Olalla Danijela Šantić R. Michael McKay Kristian Spilling Lior Guttman Petr Znachor Izabela Mujakić Lívia Kolesár Fecskeová Luca Zoccarato Martina Hanusová Andrea Pessina Tom Reich Hans-Peter Grossart Michal Koblížek
author_facet	Kasia Piwosz Ana Vrdoljak Thijs Frenken Juan Manuel González-Olalla Danijela Šantić R. Michael McKay Kristian Spilling Lior Guttman Petr Znachor Izabela Mujakić Lívia Kolesár Fecskeová Luca Zoccarato Martina Hanusová Andrea Pessina Tom Reich Hans-Peter Grossart Michal Koblížek
author_sort	Kasia Piwosz
title	Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
title_short	Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
title_full	Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
title_fullStr	Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
title_full_unstemmed	Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
title_sort	light and primary production shape bacterial activity and community composition of aerobic anoxygenic phototrophic bacteria in a microcosm experiment
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/0144a2c1fc7c4410923a2f33b43d40f3
work_keys_str_mv	AT kasiapiwosz lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT anavrdoljak lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT thijsfrenken lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT juanmanuelgonzalezolalla lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT danijelasantic lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT rmichaelmckay lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT kristianspilling lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT liorguttman lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT petrznachor lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT izabelamujakic lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT liviakolesarfecskeova lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT lucazoccarato lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT martinahanusova lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT andreapessina lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT tomreich lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT hanspetergrossart lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment AT michalkoblizek lightandprimaryproductionshapebacterialactivityandcommunitycompositionofaerobicanoxygenicphototrophicbacteriainamicrocosmexperiment
_version_	1718427865911918592

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

Ejemplares similares