Cargando…

Production and cross-feeding of nitrite within Prochlorococcus populations

Prochlorococcus is an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade of Prochlorococcus, nearly all cells can assimilate nitrite (NO(2)(−)), with a subset capable of assimilating nitrate (NO(3)(−)). LLI ce...

Descripción completa

Detalles Bibliográficos
Autores principales: Berube, Paul M., O'Keefe, Tyler J., Rasmussen, Anna, LeMaster, Trent, Chisholm, Sallie W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470740/
https://www.ncbi.nlm.nih.gov/pubmed/37404012
http://dx.doi.org/10.1128/mbio.01236-23
_version_ 1785099748030545920
author Berube, Paul M.
O'Keefe, Tyler J.
Rasmussen, Anna
LeMaster, Trent
Chisholm, Sallie W.
author_facet Berube, Paul M.
O'Keefe, Tyler J.
Rasmussen, Anna
LeMaster, Trent
Chisholm, Sallie W.
author_sort Berube, Paul M.
collection PubMed
description Prochlorococcus is an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade of Prochlorococcus, nearly all cells can assimilate nitrite (NO(2)(−)), with a subset capable of assimilating nitrate (NO(3)(−)). LLI cells are maximally abundant near the primary NO(2)(−) maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO(3)(−) reduction and subsequent NO(2)(−) release by phytoplankton. We hypothesized that some Prochlorococcus exhibit incomplete assimilatory NO(3)(−) reduction and examined NO(2)(−) accumulation in cultures of three Prochlorococcus strains (MIT0915, MIT0917, and SB) and two Synechococcus strains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO(2)(−) during growth on NO(3)(−). Approximately 20–30% of the NO(3)(−) transported into the cell by MIT0917 was released as NO(2)(−), with the rest assimilated into biomass. We further observed that co-cultures using NO(3)(−) as the sole N source could be established for MIT0917 and Prochlorococcus strain MIT1214 that can assimilate NO(2)(−) but not NO(3)(−). In these co-cultures, the NO(2)(−) released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates within Prochlorococcus populations. IMPORTANCE: Earth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations of Prochlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, some Prochlorococcus cells release extracellular NO(2)(−) during growth on NO(3)(−). In the wild, Prochlorococcus populations are composed of multiple functional types, including those that cannot use NO(3)(−) but can still assimilate NO(2)(−). We show that metabolic dependencies arise when Prochlorococcus strains with complementary NO(2)(−) production and consumption phenotypes are grown together on NO(3)(−). These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates.
format Online
Article
Text
id pubmed-10470740
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-104707402023-09-01 Production and cross-feeding of nitrite within Prochlorococcus populations Berube, Paul M. O'Keefe, Tyler J. Rasmussen, Anna LeMaster, Trent Chisholm, Sallie W. mBio Research Article Prochlorococcus is an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade of Prochlorococcus, nearly all cells can assimilate nitrite (NO(2)(−)), with a subset capable of assimilating nitrate (NO(3)(−)). LLI cells are maximally abundant near the primary NO(2)(−) maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO(3)(−) reduction and subsequent NO(2)(−) release by phytoplankton. We hypothesized that some Prochlorococcus exhibit incomplete assimilatory NO(3)(−) reduction and examined NO(2)(−) accumulation in cultures of three Prochlorococcus strains (MIT0915, MIT0917, and SB) and two Synechococcus strains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO(2)(−) during growth on NO(3)(−). Approximately 20–30% of the NO(3)(−) transported into the cell by MIT0917 was released as NO(2)(−), with the rest assimilated into biomass. We further observed that co-cultures using NO(3)(−) as the sole N source could be established for MIT0917 and Prochlorococcus strain MIT1214 that can assimilate NO(2)(−) but not NO(3)(−). In these co-cultures, the NO(2)(−) released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates within Prochlorococcus populations. IMPORTANCE: Earth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations of Prochlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, some Prochlorococcus cells release extracellular NO(2)(−) during growth on NO(3)(−). In the wild, Prochlorococcus populations are composed of multiple functional types, including those that cannot use NO(3)(−) but can still assimilate NO(2)(−). We show that metabolic dependencies arise when Prochlorococcus strains with complementary NO(2)(−) production and consumption phenotypes are grown together on NO(3)(−). These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates. American Society for Microbiology 2023-07-05 /pmc/articles/PMC10470740/ /pubmed/37404012 http://dx.doi.org/10.1128/mbio.01236-23 Text en Copyright © 2023 Berube et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Berube, Paul M.
O'Keefe, Tyler J.
Rasmussen, Anna
LeMaster, Trent
Chisholm, Sallie W.
Production and cross-feeding of nitrite within Prochlorococcus populations
title Production and cross-feeding of nitrite within Prochlorococcus populations
title_full Production and cross-feeding of nitrite within Prochlorococcus populations
title_fullStr Production and cross-feeding of nitrite within Prochlorococcus populations
title_full_unstemmed Production and cross-feeding of nitrite within Prochlorococcus populations
title_short Production and cross-feeding of nitrite within Prochlorococcus populations
title_sort production and cross-feeding of nitrite within prochlorococcus populations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470740/
https://www.ncbi.nlm.nih.gov/pubmed/37404012
http://dx.doi.org/10.1128/mbio.01236-23
work_keys_str_mv AT berubepaulm productionandcrossfeedingofnitritewithinprochlorococcuspopulations
AT okeefetylerj productionandcrossfeedingofnitritewithinprochlorococcuspopulations
AT rasmussenanna productionandcrossfeedingofnitritewithinprochlorococcuspopulations
AT lemastertrent productionandcrossfeedingofnitritewithinprochlorococcuspopulations
AT chisholmsalliew productionandcrossfeedingofnitritewithinprochlorococcuspopulations