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...
Autores principales: | , , , , |
---|---|
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 |