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Title: Production and cross-feeding of nitrite within Prochlorococcus populations
ABSTRACT

Prochlorococcusis an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus, nearly all cells can assimilate nitrite (NO2), with a subset capable of assimilating nitrate (NO3). LLI cells are maximally abundant near the primary NO2maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO3reduction and subsequent NO2release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO3reduction and examined NO2accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO2during growth on NO3. Approximately 20–30% of the NO3transported into the cell by MIT0917 was released as NO2, with the rest assimilated into biomass. We further observed that co-cultures using NO3as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO2but not NO3. In these co-cultures, the NO2released 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 withinProchlorococcuspopulations.

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 ofProchlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcuscells release extracellular NO2during growth on NO3. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO3but can still assimilate NO2. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO2production and consumption phenotypes are grown together on NO3. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates.

 
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Award ID(s):
2048470
NSF-PAR ID:
10492689
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Dubilier, Nicole
Publisher / Repository:
American Society for Microbiology
Date Published:
Journal Name:
mBio
ISSN:
2150-7511
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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