In:
mSphere, American Society for Microbiology, Vol. 4, No. 6 ( 2019-12-18)
Abstract:
Crocosphaera is a major dinitrogen (N 2 )-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N 2 -fixing enzyme nitrogenase is deactivated by oxygen (O 2 ), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O 2 management strategies by Crocosphaera sp.: size adjustment, reduced O 2 diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O 2 . Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O 2 . The model indicates a critical role for respiration in protecting the rate of N 2 fixation. Moreover, the rise in respiration rates and the decline in ambient O 2 with temperature strengthen this mechanism in warmer water, providing a physiological rationale for the observed niche of Crocosphaera at temperatures exceeding 20°C. Our new measurements of the sensitivity to light intensity show that the rate of N 2 fixation reaches saturation at a lower light intensity (∼100 μmol m −2 s −1 ) than photosynthesis and that both are similarly inhibited by light intensities of 〉 500 μmol m −2 s −1 . This suggests an explanation for the maximum population of Crocosphaera occurring slightly below the ocean surface. IMPORTANCE Crocosphaera is one of the major N 2 -fixing microorganisms in the open ocean. On a global scale, the process of N 2 fixation is important in balancing the N budget, but the factors governing the rate of N 2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O 2 and physical factors such as temperature and light affect N 2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O 2 to protect the O 2 -sensitive N 2 -fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N 2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.
Type of Medium:
Online Resource
ISSN:
2379-5042
DOI:
10.1128/mSphere.00531-19
Language:
English
Publisher:
American Society for Microbiology
Publication Date:
2019
detail.hit.zdb_id:
2844248-9
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