<i>Prochlorococcus</i> in the lab and in silico: The importance of representing exudation

Grossowicz, Michal; Roth‐Rosenberg, Dalit; Aharonovich, Dikla; Silverman, Jacob; Follows, Michael J.; Sher, Daniel

doi:10.1002/lno.10463

Cited by 28 publications

(46 citation statements)

References 85 publications

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“…3B; see also Fig. S5) (43). When entry into stationary stage was induced by N or P starvation, chlorotic cells appeared much faster, and the cultures became nonviable much earlier, i.e., essentially immediately after the cessation of exponential growth.…”

Section: Fig S3 Andmentioning

confidence: 87%

Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation

Roth‐Rosenberg

Aharonovich

Luzzatto-Knaan

et al. 2020

mBio

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Many microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by Nanoscale secondary ion mass spectrometry (NanoSIMS). However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not regrow under axenic conditions when transferred to new media. Nevertheless, cocultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Prochlorococcus. IMPORTANCE The ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions that are common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically important marine cyanobacterium. Instead, Prochlorococcus relies on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

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Section: Fig S3 Andmentioning

confidence: 87%

Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation

Roth‐Rosenberg

Aharonovich

Luzzatto-Knaan

et al. 2020

mBio

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“…202 starvation 203 To determine to what extent the macromolecular composition of Prochlorococcus changes between 204 the different physiological states of a batch culture, we grew strain MIT9312 in laboratory batch 205 cultures where the N:P ratio of the media was set to 2, thus leading to cessation of growth due to N 206 starvation (Grossowicz et al 2017). The bulk culture fluorescence, often used to monitor phytoplankton 207 growth in a non-invasive way, increased exponentially until day 10, after which the culture 208 fluorescence declined rapidly, with no clearly observable stationary stage (Fig 1a).…”

Section: Dynamics Of Cell Numbers and Macromolecular Composition Durimentioning

confidence: 99%

Dynamic macromolecular composition and high exudation rates inProchlorococcus

Roth‐Rosenberg

Aharonovich

Omta

et al. 2019

Preprint

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10Every living cell is composed of macromolecules such as proteins, DNA, RNA and pigments or 11 cofactors. The ratio between these macromolecular pools depends on the allocation of resources within 12 the organism to different physiological requirements, and in turn determines the elemental composition 13 of the organism and, potentially, how it may affect biogeochemical cycles of elements such as carbon, 14 nitrogen and phosphorus. Here, we present detailed measurements of the macromolecular composition 15 of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, 16 as it grows and declines due to N starvation in laboratory batch cultures. As cells reached stationary 17 stage and declined, protein/cell decreased by ~30% and RNA/cell and pigments/cell decreased by an 18 order of magnitude. The decline stage was associated with the appearance of chlorotic cells which had 19 higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with 20 changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-21 chlorophyll-like pigments emerged, which were not observed during exponential growth. These 22 divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern 23 Mediterranean. Around 80-85% of the carbon fixed by Prochlorococcus MIT9312 (but not of a 24 different strain, NATL2A) was released into the growth media as dissolved organic carbon under these 25 laboratory conditions. Broadly defined, the macromolecular composition of Prochlorococcus 26 MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, suggesting 27 a different set of physiological constraints determines the macromolecular composition of these two 28 broad classes of marine microorganisms. 29 30

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“…Picophytoplankton, including cyanobacteria (Prochlorococcus and Synechococcus) and picoeukaryotes, account for a large portion of algal biomass and primary productivity in LNLC systems [41,[54][55][56][57]. Two factors that drive picophytoplankton abundance in LNLC regions are (1) nutrient availability [58,59], and (2) population decline through viral infections and lysis [60]. Previous studies have shown that atmospheric deposition affects picophytoplankton variably, both increasing abundance due to a supply of nutrients [45][46][47] and decreasing abundance due to a supply of toxic metals [20].…”

Section: Impact Of Airbone Microbes (Or Dust Deposition) On Phytoplanmentioning

confidence: 99%

Dust-Associated Airborne Microbes Affect Primary and Bacterial Production Rates, and Eukaryotes Diversity, in the Northern Red Sea: A Mesocosm Approach

et al. 2019

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The northern Red Sea (NRS) is a low-nutrient, low-chlorophyll (LNLC) ecosystem with high rates of atmospheric deposition due to its proximity to arid regions. Impacts of atmospheric deposition on LNLC ecosystems have been attributed to the chemical constituents of dust, while overlooking bioaerosols. Understanding how these vast areas of the ocean will respond to future climate and anthropogenic change hinges on the response of microbial communities to these changes. We tested the impacts of bioaerosols on the surface water microbial diversity and the primary and bacterial production rates in the NRS, a system representative of other LNLC oceanic regions, using a mesocosm bioassay experiment. By treating NRS surface seawater with dust, which contained nutrients, metals, and viable organisms, and “UV-treated dust” (which contained only nutrients and metals), we were able to assess the impacts of bioaerosols on local natural microbial populations. Following amendments (20 and 44 h) the incubations treated with “live dust” showed different responses than those with UV-treated dust. After 44 h, primary production was suppressed (as much as 50%), and bacterial production increased (as much as 55%) in the live dust treatments relative to incubations amended with UV-treated dust or the control. The diversity of eukaryotes was lower in treatments with airborne microbes. These results suggest that the airborne microorganisms and viruses alter the surface microbial ecology of the NRS. These results may have implications for the carbon cycle in LNLC ecosystems, which are expanding and are especially important since dust storms are predicted to increase in the future due to desertification and expansion of arid regions.

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Prochlorococcus in the lab and in silico: The importance of representing exudation

Cited by 28 publications

References 85 publications

Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation

Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation

Dynamic macromolecular composition and high exudation rates inProchlorococcus

Dust-Associated Airborne Microbes Affect Primary and Bacterial Production Rates, and Eukaryotes Diversity, in the Northern Red Sea: A Mesocosm Approach

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