Cargando…

Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System

B vitamins are essential cofactors for practically all living organisms on Earth and are produced by a selection of microorganisms. An imbalance between high demand and limited production, in concert with abiotic processes, may explain the low availability of these vitamins in marine systems. Natura...

Descripción completa

Detalles Bibliográficos
Autores principales: Joglar, Vanessa, Pontiller, Benjamin, Martínez-García, Sandra, Fuentes-Lema, Antonio, Pérez-Lorenzo, María, Lundin, Daniel, Pinhassi, Jarone, Fernández, Emilio, Teira, Eva
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552899/
https://www.ncbi.nlm.nih.gov/pubmed/34495690
http://dx.doi.org/10.1128/AEM.01525-21
_version_ 1784591476090470400
author Joglar, Vanessa
Pontiller, Benjamin
Martínez-García, Sandra
Fuentes-Lema, Antonio
Pérez-Lorenzo, María
Lundin, Daniel
Pinhassi, Jarone
Fernández, Emilio
Teira, Eva
author_facet Joglar, Vanessa
Pontiller, Benjamin
Martínez-García, Sandra
Fuentes-Lema, Antonio
Pérez-Lorenzo, María
Lundin, Daniel
Pinhassi, Jarone
Fernández, Emilio
Teira, Eva
author_sort Joglar, Vanessa
collection PubMed
description B vitamins are essential cofactors for practically all living organisms on Earth and are produced by a selection of microorganisms. An imbalance between high demand and limited production, in concert with abiotic processes, may explain the low availability of these vitamins in marine systems. Natural microbial communities from surface shelf water in the productive area off northwestern Spain were enclosed in mesocosms in winter, spring, and summer 2016. In order to explore the impact of B-vitamin availability on microbial community composition (16S and 18S rRNA gene sequence analysis) and bacterial function (metatranscriptomics analysis) in different seasons, enrichment experiments were conducted with seawater from the mesocosms. Our findings revealed that significant increases in phytoplankton or prokaryote biomass associated with vitamin B(12) and/or B(1) amendments were not accompanied by significant changes in community composition, suggesting that most of the microbial taxa benefited from the external B-vitamin supply. Metatranscriptome analysis suggested that many bacteria were potential consumers of vitamins B(12) and B(1), although the relative abundance of reads related to synthesis was ca. 3.6-fold higher than that related to uptake. Alteromonadales and Oceanospirillales accounted for important portions of vitamin B(1) and B(12) synthesis gene transcription, despite accounting for only minor portions of the bacterial community. Flavobacteriales appeared to be involved mostly in vitamin B(12) and B(1) uptake, and Pelagibacterales expressed genes involved in vitamin B(1) uptake. Interestingly, the relative expression of vitamin B(12) and B(1) synthesis genes among bacteria strongly increased upon inorganic nutrient amendment. Collectively, these findings suggest that upwelling events intermittently occurring during spring and summer in productive ecosystems may ensure an adequate production of these cofactors to sustain high levels of phytoplankton growth and biomass. IMPORTANCE B vitamins are essential growth factors for practically all living organisms on Earth that are produced by a selection of microorganisms. An imbalance between high demand and limited production may explain the low concentration of these compounds in marine systems. In order to explore the impact of B-vitamin availability on bacteria and algae in the coastal waters off northwestern Spain, six experiments were conducted with natural surface water enclosed in winter, spring, and summer. Our findings revealed that increases in phytoplankton or bacterial growth associated with B(12) and/or B(1) amendments were not accompanied by significant changes in community composition, suggesting that most microorganisms benefited from the B-vitamin supply. Our analyses confirmed the role of many bacteria as consumers of vitamins B(12) and B(1), although the relative abundance of genes related to synthesis was ca. 3.6-fold higher than that related to uptake. Interestingly, prokaryote expression of B(12) and B(1) synthesis genes strongly increased when inorganic nutrients were added. Collectively, these findings suggest that upwelling of cold and nutrient-rich waters occurring during spring and summer in this coastal area may ensure an adequate production of B vitamins to sustain high levels of algae growth and biomass.
format Online
Article
Text
id pubmed-8552899
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-85528992021-11-12 Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System Joglar, Vanessa Pontiller, Benjamin Martínez-García, Sandra Fuentes-Lema, Antonio Pérez-Lorenzo, María Lundin, Daniel Pinhassi, Jarone Fernández, Emilio Teira, Eva Appl Environ Microbiol Environmental Microbiology B vitamins are essential cofactors for practically all living organisms on Earth and are produced by a selection of microorganisms. An imbalance between high demand and limited production, in concert with abiotic processes, may explain the low availability of these vitamins in marine systems. Natural microbial communities from surface shelf water in the productive area off northwestern Spain were enclosed in mesocosms in winter, spring, and summer 2016. In order to explore the impact of B-vitamin availability on microbial community composition (16S and 18S rRNA gene sequence analysis) and bacterial function (metatranscriptomics analysis) in different seasons, enrichment experiments were conducted with seawater from the mesocosms. Our findings revealed that significant increases in phytoplankton or prokaryote biomass associated with vitamin B(12) and/or B(1) amendments were not accompanied by significant changes in community composition, suggesting that most of the microbial taxa benefited from the external B-vitamin supply. Metatranscriptome analysis suggested that many bacteria were potential consumers of vitamins B(12) and B(1), although the relative abundance of reads related to synthesis was ca. 3.6-fold higher than that related to uptake. Alteromonadales and Oceanospirillales accounted for important portions of vitamin B(1) and B(12) synthesis gene transcription, despite accounting for only minor portions of the bacterial community. Flavobacteriales appeared to be involved mostly in vitamin B(12) and B(1) uptake, and Pelagibacterales expressed genes involved in vitamin B(1) uptake. Interestingly, the relative expression of vitamin B(12) and B(1) synthesis genes among bacteria strongly increased upon inorganic nutrient amendment. Collectively, these findings suggest that upwelling events intermittently occurring during spring and summer in productive ecosystems may ensure an adequate production of these cofactors to sustain high levels of phytoplankton growth and biomass. IMPORTANCE B vitamins are essential growth factors for practically all living organisms on Earth that are produced by a selection of microorganisms. An imbalance between high demand and limited production may explain the low concentration of these compounds in marine systems. In order to explore the impact of B-vitamin availability on bacteria and algae in the coastal waters off northwestern Spain, six experiments were conducted with natural surface water enclosed in winter, spring, and summer. Our findings revealed that increases in phytoplankton or bacterial growth associated with B(12) and/or B(1) amendments were not accompanied by significant changes in community composition, suggesting that most microorganisms benefited from the B-vitamin supply. Our analyses confirmed the role of many bacteria as consumers of vitamins B(12) and B(1), although the relative abundance of genes related to synthesis was ca. 3.6-fold higher than that related to uptake. Interestingly, prokaryote expression of B(12) and B(1) synthesis genes strongly increased when inorganic nutrients were added. Collectively, these findings suggest that upwelling of cold and nutrient-rich waters occurring during spring and summer in this coastal area may ensure an adequate production of B vitamins to sustain high levels of algae growth and biomass. American Society for Microbiology 2021-10-28 /pmc/articles/PMC8552899/ /pubmed/34495690 http://dx.doi.org/10.1128/AEM.01525-21 Text en Copyright © 2021 Joglar 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 Environmental Microbiology
Joglar, Vanessa
Pontiller, Benjamin
Martínez-García, Sandra
Fuentes-Lema, Antonio
Pérez-Lorenzo, María
Lundin, Daniel
Pinhassi, Jarone
Fernández, Emilio
Teira, Eva
Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title_full Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title_fullStr Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title_full_unstemmed Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title_short Microbial Plankton Community Structure and Function Responses to Vitamin B(12) and B(1) Amendments in an Upwelling System
title_sort microbial plankton community structure and function responses to vitamin b(12) and b(1) amendments in an upwelling system
topic Environmental Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552899/
https://www.ncbi.nlm.nih.gov/pubmed/34495690
http://dx.doi.org/10.1128/AEM.01525-21
work_keys_str_mv AT joglarvanessa microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT pontillerbenjamin microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT martinezgarciasandra microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT fuenteslemaantonio microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT perezlorenzomaria microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT lundindaniel microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT pinhassijarone microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT fernandezemilio microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem
AT teiraeva microbialplanktoncommunitystructureandfunctionresponsestovitaminb12andb1amendmentsinanupwellingsystem