Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms

Diner, Rachel E.; Schwenck, Sarah M.; McCrow, John P.; Zheng, Hong; Allen, Andrew E.

doi:10.3389/fmicb.2016.00880

Title: Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms

Journal Article · Thu Jun 09 00:00:00 EDT 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.00880· OSTI ID:1287173

Diner, Rachel E. ^[1]; Schwenck, Sarah M. ^[1]; McCrow, John P. ^[2]; Zheng, Hong ^[2]; Allen, Andrew E. ^[1]

Univ. of California San Diego, La Jolla, CA (United States). Integrative Oceanography Division, Scripps Institution of Oceanography; J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group

Diatoms are a dominant group of eukaryotic phytoplankton that contribute substantially to global primary production and the cycling of important elements such as carbon and nitrogen. Heterotrophic bacteria, including members of the gammaproteobacteria, are commonly associated with diatom populations and may rely on them for organic carbon while potentially competing with them for other essential nutrients. Considering that bacterioplankton drive oceanic release of CO2 (i.e., bacterial respiration) while diatoms drive ocean carbon sequestration vial the biological pump, the outcome of such competition could influence the direction and magnitude of carbon flux in the upper ocean. Nitrate availability is commonly a determining factor for the growth of diatom populations, particularly in coastal and upwelling regions. Diatoms as well as many bacterial species can utilize nitrate, however the ability of bacteria to compete for nitrate may be hindered by carbon limitation. Here we have developed a genetically tractable model system using the pennate diatom Phaeodactylurn tricomuturn and the widespread heterotrophic bacteria Alterornonas macleodii to examine carbon-nitrogen dynamics. While subsisting solely on P tricomutum derived carbon. A. macleodii does not appear to be an effective competitor for nitrate, and may in fact benefit the diatom; particularly in stationary phase. However, allochthonous dissolved organic carbon addition in the form of pyruvate triggers A. macleodir proliferation and nitrate uptake, leading to reduced P tricornutum growth. Nitrate reductase deficient mutants of A, macleodii (AnasA) do not exhibit such explosive growth and associated competitive ability in response to allochthonous carbon when nitrate is the sole nitrogen source, but could survive by utilizing solely P tricomutum-derived nitrogen. Furthermore, allocthonous carbon addition enables wild-type A. macleodil to rescue nitrate reductase deficient P tricomutum populations from nitrogen starvation, and RNA-seq transcriptomic evidence supports nitrogen-based interactions between diatoms and bacteria at the molecular level. This study provides key insights into the roles of carbon and nitrogen in phytoplankton-bacteria dynamics and lays the foundation for developing a mechanistic understanding of these interactions using co-culturing and genetic manipulation.

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Research Organization:: Univ. of California, San Diego, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Gordon and Betty Moore Foundation; National Science Foundation (NSF)

Grant/Contract Number:: SC0008593; GBMF3828; GBMF5006; OCE-1136477

OSTI ID:: 1287173

Alternate ID(s):: OSTI ID: 1438053

Journal Information:: Frontiers in Microbiology, Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii Koch, Hanna; Germscheid, Nora; Freese, Heike M. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57526-5	journal	January 2020
A synthetic microbial loop for modelling heterotroph-phototroph metabolic interactions Fondi, Marco; Di Patti, Francesca Ecological Modelling https://doi.org/10.1101/379131	journal	July 2018
Ecological Energetic Perspectives on Responses of Nitrogen-Transforming Chemolithoautotrophic Microbiota to Changes in the Marine Environment Dang, Hongyue; Chen, Chen-Tung A. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01246	journal	July 2017
Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise Hou, Shengwei; López-Pérez, Mario; Pfreundt, Ulrike ETH Zurich https://doi.org/10.3929/ethz-b-000235594	text	January 2018
More than stoichiometry: the molecular composition of inorganic and organic substrates controls ammonium regeneration by bacteria Guo, J.; Cherif, M. Aquatic Ecology https://doi.org/10.1101/2020.03.17.996322	journal	March 2020

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59 BASIC BIOLOGICAL SCIENCES
diatoms
bacteria
nitrate
competition
genetic manipulation
transcriptomics
Phaeodactylum
Alteromonas
dissolved organic nitrogen
whole-cell response
phaeodactylum-tricornutum
alteromonas-macleodii
marine-bacteria
phytoplankton cultures
assimilation genes
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