Survival of <i>Prochlorococcus</i> in extended darkness

Coe, Allison; Ghizzoni, Julie; LeGault, Kristen N.; Biller, Steven J.; Roggensack, Sara E.; Chisholm, Sallie W.

doi:10.1002/lno.10302

Cited by 68 publications

(109 citation statements)

References 78 publications

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“…day 34 in Figure 3). This is consistent with a previous study showing that cells belonging to a 176 different Prochlorococcus strain, MED4, that were incubated for three days in the dark, were unable to 177 resume growth after return to light despite showing no clear difference in the chlorophyll 178 autofluorescence (Coe et al 2016). The probability of growth after transfer did not depend on the 179 number of transferred cells (Morris et al 2008), with as many as 2.5×10 7 cells/ml failing to grow after 180 transfer during culture decline (cells at ~1/10 of this density grew after being transferred during 181 exponential stage).…”

Section: Evaluating the Viability Of Sub-populations 169supporting

confidence: 89%

Prochlorococcusrely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

Roth‐Rosenberg

Aharonovich

Luzzatto-Knaan

et al. 2019

Preprint

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24Many microorganisms produce resting cells with very low metabolic activity that allow them to 25 survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic 26 phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic 27 pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under 28 multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant 29 phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean 30 biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced 31 metabolic activity, measured as C and N uptake by NanoSIMS. However, unlike many other 32 cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not re-grow under axenic 33 conditions when transferred to new media. Nevertheless, co-cultures with a heterotrophic 34 bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient 35 starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather 36 than the ability to survive extended starvation as resting cells, underlies the ecological success 37 of Prochlorococcus. 38 39 Importance 40 The ability of microorganisms to withstand long periods of nutrient starvation is key to their 41 survival and success under highly fluctuating conditions as is common in nature. Therefore, one 42 would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. 43 Here, we show that this is not the case for Prochlorococcus, a globally abundant and 44 3 ecologically impactful marine cyanobacterium. Instead, Prochlorococcus rely on co-occurring 45 heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results 46 highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean 47 and elsewhere with consequences at the global scale. 48 49

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Section: Evaluating the Viability Of Sub-populations 169supporting

confidence: 89%

Prochlorococcusrely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

Roth‐Rosenberg

Aharonovich

Luzzatto-Knaan

et al. 2019

Preprint

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“…discussed in detail below, Fig S1, see also(Coe et al 2016, Roth-Rosenberg et al 2019)). We did not 308 measure the amount of the macromolecular pools in each sub-population separately, due to the 309 difficulty in obtaining sufficient biomass from non-fixed cells sorted by fluorescence-activated cell 310 sorting.…”

mentioning

confidence: 88%

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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“…This observation suggests that light conditions below the mixed layer may be dynamic in previously unrecognized ways (i.e., non-diel patterns) due to processes such as turbulent mixing at the mixed layer to thermocline interface, breaking of internal waves, light shock, and long periods of darkness. Indeed, recent laboratory experiments show that Prochlorococcus in the company of heterotrophic bacteria can survive prolonged darkness (Coe et al, 2016). More work examining how Prochlorococcus responds to non-diel light fluctuations is needed to more deeply understand the ecology of this abundant cyanobacterium.…”

Section: Chlorophyll Physiology Cannot Be Fully Explained By Communitmentioning

confidence: 99%

Dynamics of Prochlorococcus Diversity and Photoacclimation During Short-Term Shifts in Water Column Stratification at Station ALOHA

Thompson

Engh²,

Ahlgren

et al. 2018

Front. Mar. Sci.

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The cyanobacterium Prochlorococcus is the dominant phototroph in surface waters of the vast oligotrophic oceans, the foundation of marine food webs, and an important component of global biogeochemical cycles. The prominence of Prochlorococcus across the environmental gradients of the open ocean is attributed to its extensive genetic diversity and flexible chlorophyll physiology, enabling light capture over a wide range of intensities. What remains unknown is the balance between temporal dynamics of genetic diversity and chlorophyll physiology in the ability of Prochlorococcus to respond to a variety of short (approximately 1 day) and longer (months to year) changes in the environment. Previous field research established depth-dependent Prochlorococcus single cell chlorophyll distributions in the North Pacific Subtropical Gyre. Here, we examined whether the shifts in chlorophyll distributions correspond to changes in Prochlorococcus genetic diversity (i.e., ecotype-level community structure) or photoacclimation of stable communities over short time intervals. We report that community structure was relatively stable despite abrupt shifts in Prochlorococcus chlorophyll physiology, due to unexpected physiological plasticity of high-light adapted Prochlorococcus ecotypes. Through comparison with seasonalscale changes, our data suggest that variability on daily scales triggers shifts in Prochlorococcus photoacclimation, while seasonal-scale dynamics trigger shifts in community structure. Together, these data highlight the importance of incorporating the process of photoacclimation and chlorophyll dynamics into interpretations of phytoplankton population dynamics from chlorophyll data as well as the importance of daily-scale variability to Prochlorococcus ecology.

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Survival of Prochlorococcus in extended darkness

Cited by 68 publications

References 78 publications

Prochlorococcusrely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

Prochlorococcusrely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

Dynamic macromolecular composition and high exudation rates inProchlorococcus

Dynamics of Prochlorococcus Diversity and Photoacclimation During Short-Term Shifts in Water Column Stratification at Station ALOHA

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