Biology subjects

Aharonovich, D.

Publications and source records attributed to Aharonovich, D..

16 recordsLinked to original sources

bioRxiv2025

Transcriptomic and Proteomic Analysis Reveals Nitrogen Recycling as a Core Mechanism for Prochlorococcus Prolonged Survival

Prochlorococcus, the dominant cyanobacterium in the oligotrophic ocean, possesses a streamlined genome and depends on interactions with heterotrophic bacteria for survival under various stressors. While the role of helper bacteria in mitigating oxidative stress is established, the mechanisms enabling its long-term survival under nitrogen (N) limitation remain poorly characterized. Here, we employ a multi-omics approach--integrating transcriptomics and proteomics--to investigate the physiological processes that facilitate the prolonged survival of Prochlorococcus in co-culture with the marine heterotroph Alteromonas during conditions of extreme N-deprivation. Our results demonstrate that, unlike axenic cultures which rapidly perish, Prochlorococcus in co-culture maintains viability for months following the depletion of initial N-sources. Molecular analysis identifies a shift in both organisms that underpins this persistence: Prochlorococcus strongly upregulates high-affinity N-scavenging pathways, while Alteromonas exhibits transcriptional and translational changes consistent with increased organic matter degradation and reduced motility. This suggests that Alteromonas functions as a key nitrogen recycler, providing a continuous, albeit low-level, supply of bioavailable NH4+ to its photoautotrophic partner through the remineralization of organic matter. These findings support and extend the Black Queen Hypothesis, illustrating that the benefits conferred by heterotrophs to genome-streamlined primary producers encompass not only the detoxification of reactive oxygen species but also the continuous provisioning of essential macro-nutrients under starvation conditions. This tightly coupled, mutualistic relationship represents a critical factor driving the resilience and productivity of microbial communities in oligotrophic marine ecosystems.

microbiology↗

bioRxiv2025

Distinct microbial response to organic matter from nitrogen-starved and virus-infected phytoplankton

When phytoplankton die they release dissolved organic matter (DOM) that feeds co-occurring heterotrophic bacteria. We show that death due to phage infection and nitrogen starvation result in different changes to the macromolecular structure of Prochlorococcus, a globally abundant cyanobacterium, and that the resulting DOM elicits different microbial responses. Viral infection led to increased RNA and DNA content in Prochlorococcus whereas nitrogen starvation led to a lower protein content. DOM released from phage-infected cells induced high secondary (bacterial) production, while DOM from starved cells increased dark (heterotrophic) primary production in natural microbial communities from the oligotrophic Eastern Mediterranean Sea. Through 16S and 18S amplicon sequencing, metagenomics, and laboratory experiments we identify Alteromonadaceae and Rhodobacteraceae as heterotrophic taxa responding differently to the two DOM sources. We propose that distinct forms of phytoplankton mortality drive shifts in microbial community metabolism, including differential activity of pathways for heterotrophic carbon fixation, likely through anaplerotic reactions.

microbiology↗

bioRxiv2025

Dynamics of cell death due to N and P starvation across intra-clade diversity in Prochlorococcus

Nutrient starvation and subsequent mortality are processes that can shape ecosystem dynamics and influence global biogeochemical cycles yet are poorly understood. Here, we examined the dynamics of culture decline in 15 strains of Prochlorococcus, globally abundant marine cyanobacteria, under nitrogen (N) and phosphate (P) starvation. We then ask whether mortality patterns can be related to the evolutionary history of each strain, the geographic location and environmental conditions where it was isolated from, or the copy number of specific acquisition genes. We observed diverse decline patterns across starvation conditions and strains, identifying three differential features: maximum culture fluorescence, the number of fluorescence peaks during the decline stage, and the decline rate. Based on these features, each strain was categorized as being more sensitive to either nitrogen starvation or phosphorus/co-starvation. High light (HL) strains are more sensitive to N starvation, whereas other facets of the strains evolutionary or ecological origin were not correlated with mortality features. Surprisingly, the number of genes known to be involved in either N or P acquisition in each genome was not correlated with starvation sensitivity. Rather, genes involved in DNA damage repair were associated with N sensitivity to starvation, especially in HL strains, whereas genes related to protein quality control were more abundant in LL strains and associated with P/co starvation sensitivity. These findings reveal a previously unrecognized diversity in the dynamics of starvation and mortality across closely related Prochlorococcus strains, potentially driven by differences in the responses to DNA and protein damage.

microbiology↗

bioRxiv2025

Four Potential Mechanisms Underlying Phytoplankton-Bacteria Interactions Assessed Using Experiments and Models

Phytoplankton growth and death depend on interactions with heterotrophic bacteria, yet the underlying mechanisms remain mostly unclear. We ask whether mathematical models explicitly representing four putative mechanisms of interaction (overflow metabolism, mixotrophy, exoenzymes and ROS detoxification) can recapitulate laboratory co-cultures between Prochlorococcus and 8 heterotrophic bacteria, ranging from synergism to antagonism. Two fundamentally distinct modes of interaction emerge from the models: i) Organic carbon and nitrogen recycling through exoenzymes or overflow metabolism, where high biomass of both organisms leads to more productive systems and more recalcitrant organic matter. ii) Detoxification of ROS, where a small number of "exploited" heterotrophs are sufficient to support Prochlorococcus survival. Cross feeding is likely more common in laboratory co-cultures, and most models cannot reproduce total inhibition of Prochlorococcus, suggesting additional mechanisms such as allelopathy. Key model parameters determining co-culture outcome are related to cell death and biomass recycling, providing priorities for future research.

microbiology↗

bioRxiv2024

Jellyfish blooms Through the Microbial Lens: Temporal Changes, Cross-Species and Jellyfish-Water Comparisons

In this study, we explore the dynamics of bacterial communities associated with Rhopilema nomadica blooms, the predominant jellyfish in the Eastern Mediterranean Sea. We collected over 120 samples from more than 30 individuals across five major bloom events, capturing both lesser-studied winter blooms and the peaks and declines of summer blooms. Our analysis revealed significant microbial shifts-increases in Endozoicomonas and unclassified Rickettsiales were significantly more abundance during late summer blooms, while Tenacibaculum dominated in winter. Additionally, we examined microbial patterns within specific tissues--bell, gonads, tentacles, and gastrovascular system--to assess variations across these different niches. This revealed high relative abundance of specific taxa tailored to different tissue-Bacteroides was predominantly found in the bell, Simkaniaceae in the gonads, and Endozoicomonas in the tentacles. Further expanding our research, we compared the top taxa of R. nomadica with those of nine other jellyfish species from different locations. Interestingly, while no universal core microbiome was found, several taxa, including Endozoicomonas, Mycoplasma, and Spiroplasma, were common across different species, suggesting their potential ecological roles across jellyfish. Lastly, our study of potential bacterial transmission modes revealed that key bacteria associated with R. nomadica are exclusively found near bloom areas, and are absent from remote seawater, highlighting potential localized transmission dynamics between jellyfish and their immediate marine environment. Our study marks the first exploration of microbial dynamics within R. nomadica, while also broadening the understanding of other jellyfish microbial communities and setting the stage for future studies to delve deeper into their complex interactions. IMPORTANCEJellyfish blooms, like those of Rhopilema nomadica in the Eastern Mediterranean, impact marine ecosystems and human industries. Understanding the complex relationships between jellyfish and their microbiomes is important, as these interactions may influence bloom formation and decline. Our study explores microbiome variations across different stages of R. nomadica blooms, identifies common bacteria among jellyfish from various locations, and examines potential transmission modes of the main jellyfish-associated bacteria. Microbial communities vary significantly between bloom stages and jellyfish tissues, becoming less diverse towards the end of the bloom. Although no universal core microbiome was discovered, taxa such as Endozoicomonas, Mycoplasma, and Spiroplasma are prevalent across various jellyfish, suggesting significant ecological roles. Finally, our findings indicate that key bacteria associated with R. nomadica predominantly reside near bloom areas and are absent from distant seawater, highlighting localized transmission mode. This study enhances our understanding of jellyfish-associated microbial communities and their role in bloom dynamics.

microbiology↗

bioRxiv2024

Diversity in the Utilization of Different Molecular Classes of Dissolved Organic Matter by Heterotrophic Marine Bacteria

Heterotrophic marine bacteria utilize and recycle dissolved organic matter (DOM), impacting biogeochemical cycles. It is currently unclear to what extent distinct DOM components can be utilized by different heterotrophic clades. Here, we ask how a natural microbial community from the Eastern Mediterranean Sea responds to different molecular classes of DOM. These molecular classes - peptides, amino acids, amino sugars, disaccharides, monosaccharides and organic acids - together comprise much of the biomass of living organisms, released upon their death as DOM. Bulk bacterial activity increased after 24-hours for all treatments relative to the control, while glucose and ATP uptake decreased or remained unchanged. The relative abundance of several bacterial families, assessed using 16S rRNA amplicon sequencing, increased in some treatments: peptides promoted an increase in Pseudoalteromonadaceae, disaccharides promoted both Pseudoalteromonadaceae and Alteromonadaceae, and most other treatments were dominated by Vibrionaceae. While some results were consistent with recent laboratory-based studies, for example Pseudoalteromonadaceae favoring peptides, other clades behaved differently. Alteromonadaceae, for example, grew well in the lab on many substrates but dominated in seawater samples when disaccharides were added. These results highlight the diversity in DOM utilization among heterotrophic bacteria and complexities in the response of natural communities. ImportanceThe marine DOM pool contains numerous molecular classes, which change depending on the phytoplankton species, environmental conditions and interactions with other microbes, viruses and predators. In turn, the availability of these macromolecular pools affects the composition and function of the whole microbial community. Tracing the path between different carbon sources to specific microbes is another step towards revealing the dynamic interaction between bacteria and the DOM pool. This is especially important in warm and oligotrophic marine systems (e.g., Eastern Mediterranean Sea) where nutrients are scarce and may therefore affect microbial activity and growth.

microbiology↗

bioRxiv2022

An Interplay of Phytoplankton Donor Species and Transformation of Released Compounds over Time Defines Bacterial Communities Following Phytoplankton DOMp Pulses

Phytoplankton-bacteria interactions are stimulated by phytoplankton-released dissolved organic matter (DOMp). Two factors that shape the accompanying bacterial community are i) the "donor" phytoplankton species, defining the initial composition of released DOMp, and ii) the DOMp transformation over time. We added phytoplankton DOM from two globally abundant species - the diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus MIT9312 - to natural bacterial communities in the Eastern Mediterranean and determined the bacterial responses over a time-course of 72 h in terms of cell numbers, bacterial production (BP), alkaline phosphatase activity (APA), and changes in active bacterial community compositions based on rRNA amplicon sequencing. Both DOMp types were demonstrated to serve the bacterial community as carbon and potentially phosphorus source. Diatom-derived DOM induced higher BP and lower APA compared to cyanobacterium DOM after 24 h, but not after 48 and 72 h of incubation, and also maintained higher Shannon diversities over the course of the experiment, indicating a better bacterial accessibility and broader disposability of diatom derived DOM. Bacterial communities significantly differed between DOMp types as well as different incubation times, pointing to a certain bacterial specificity for the DOMp donor as well as a successive utilization of phytoplankton DOM by different bacterial taxa. The highest differences in bacterial community composition with DOMp types occurred shortly after additions, suggesting a high specificity towards highly bioavailable DOMp compounds. We conclude that phytoplankton associated bacterial communities are strongly shaped by an interplay between phytoplankton donor and the transformation of its released DOMp over time. IMPORTANCEPhytoplankton-bacteria interactions maintain biogeochemical cycles of global importance. Phytoplankton photosynthetically fix carbon dioxide and subsequently release the synthesized compounds as dissolved organic matter (DOMp), which becomes processed and recycled by heterotrophic bacteria. Yet, the combined effect of the phytoplankton donor species and time-dependent transformation of DOMp compounds on the accessibility to the bacterial community has not been explored until now. The diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus MIT9312 are globally important phytoplankton species, and our study revealed that DOMp of both species was selectively incorporated by the bacterial community. The donor species had the highest impact shortly after DOMp appropriation, and its effect diminished over time. Our results improve the understanding of biogeochemical cycles between phytoplankton and bacteria, and solve yet unresolved questions of phytoplankton-bacteria interactions.

microbiology↗

bioRxiv2022

Selecting 16S rRNA primers for microbiome analysis in a host-microbe system: the case of the jellyfish Rhopilema nomadica

Amplicon sequencing of the 16S rRNA gene is extensively used to characterize bacterial communities, including those living in association with eukaryotic hosts. Deciding which region of the 16S rRNA gene to analyze and selecting the appropriate PCR primers remained a major decision when initiating any new microbiome study. Here, we compared three commonly used primers targeting different hypervariable regions of the 16S rRNA gene, V1V2, V3V4, and V4V5, using the jellyfish Rhopilema nomadica as a model. Although all primers exhibit a similar pattern in bacterial community composition, the performance of the V3V4 primer set was superior to V1V2 and V4V5. The V1V2 primers misclassified bacteria from the Bacilli class and exhibited low classification resolution for Rickettsiales, which represent the second most abundant 16S rRNA gene sequence in all the primers. The V4V5 primer set detected almost the same community composition as the V3V4, but the ability of these primers to also amplify eukaryotic 18S rRNA gene may hinder bacterial community observations. However, after overcoming the challenges possessed by each one of those primers, we found that all three of them show very similar bacterial community dynamics and composition. Nevertheless, based on our results, we propose that the V3V4 primer set is the most suitable for studying jellyfish-associated bacterial communities. Our results suggest that, at least for jellyfish samples, it may be feasible to directly compare microbial community estimates from different studies, each using different primers but otherwise similar experimental protocols. More generally, we recommend specifically testing different primers as a prelude to large-scale 16S rRNA gene amplicon analyses, especially of previously unstudied host-microbe associations.

microbiology↗

bioRxiv2022

Significant organic carbon acquisition by Prochlorococcus in the oceans

Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon but the relative contribution of these two carbon sources is not well quantified. Here, single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea are obtaining only ~20% of carbon required for growth by photosynthesis. Consistently, laboratory-calibrated evaluations of Prochlorococcus photosynthesis indicate that carbon fixation is systematically too low to support published in situ growth rates in the deep photic layer of the Pacific Ocean. Furthermore, agent-based model simulations show that mixotrophic cells maintain realistic growth rates and populations 10s of meters deeper than obligate photo-autotrophs, deepening the nutricline and Deep Chlorophyll Maximum by ~20 m. Time-series of Prochlorococcus ecotype-abundance from the subtropical North Atlantic and North Pacific suggest that up to 30% of the Prochlorococcus cells live where light intensity is not enough to sustain obligate photo-autotrophic populations during warm, stratified periods. Together, these data and models suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.

microbiology↗

bioRxiv2021

Phototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversity

Microbial interactions such as those between phytoplankton and bacteria been studied intensively using specific model organisms, due to their potential impact on ecosystems and biogeochemistry. Yet, to what extent interactions differ between closely related organisms, or how these interactions change over time or culture conditions, remains unclear. Here, we characterize the interactions between five strains each of two globally abundant marine microorganisms, Prochlorococcus (a phototroph) and Alteromonas (a heterotroph), from the first encounter between individual strains and over more than a year of repeated cycles of exponential growth and long-term nitrogen starvation. Prochlorococcus-Alteromonas interactions had little effect on traditional growth parameters such as Prochlorococcus growth rate, maximal fluorescence or lag phase, affecting primarily the dynamics of culture decline, which we interpret as representing cell mortality and lysis. The shape of the Prochlorococcus decline curve and the carrying capacity of the co-cultures were determined by the phototroph and not the heterotroph strains involved. Comparing various mathematical models of culture mortality suggests that Prochlorococcus death rate increases over time in mono-cultures but decreases in co-cultures, with cells potentially becoming more resistant to stress. Our results demonstrate intra-species differences in ecologically-relevant co-culture outcomes. These include the recycling efficiency of N and whether the interactions are mutually synergistic or competitive. They also highlight the information-rich growth and death curves as a useful readout of the interaction phenotype. Significance StatementInteractions between phytoplankton and marine bacteria impact global ecosystems and biogeochemistry. Here, we explore how intra-species variability affects the interactions between Prochlorococcus, a globally abundant photosynthetic cyanobacetrium and Alteromonas, a heterotrophic bacterium that lives off and recycles organic matter. Under nitrogen starvation, Prochlorococcus growing alone increasingly accumulate damage and die, whereas in co-culture with Alteromonas they become increasingly resilient. The specific Prochlorococcus strain had a much larger effect on co-culture behavior than the Alteromonas strain, determining whether the interactions are mutually synergistic or potentially competitive. These results show how ecologically relevant outcomes of interactions may vary between closely related microorganisms, and highlight growth and death curves from laboratory (co)-cultures as information-rich views of microbial growth and death.

microbiology↗

bioRxiv2021

Phytoplankton exudates provide full nutrition to a subset of accompanying heterotrophic bacteria via carbon, nitrogen and phosphorus allocation

Marine bacteria rely on phytoplankton exudates as carbon sources (DOCp). Yet, it is unclear to what extent phytoplankton exudates also provide nutrients such as phytoplankton-derived N and P (DONp, DOPp). We address these questions by exudate addition experiments from the ubiquitous pico-cyanobacterium Prochlorococcus to contrasting ecosystems in the Eastern Mediterranean - a coastal and an open-ocean, oligotrophic station. Nutrient addition did not lower the incorporation of exudate DONp, nor did it reduce alkaline phosphatase activity, suggesting that bacterial communities are able to exclusively cover their nitrogen and phosphorus demands with organic forms provided by phytoplankton exudates. Approximately half of the cells in each ecosystem took up detectable amounts of Prochlorococcus-derived C and N, yet based on 16S rRNA sequencing different bacterial genera were responsible for the observed exudate utilization patterns. In the coastal community, several phylotypes of Aureimarina, Psychrosphaera and Glaciecola responded positively to the addition of phytoplankton exudates, whereas phylotypes of Pseudoalteromonas increased and dominated the open ocean communities. Together, our results strongly indicate that phytoplankton exudates provide coastal and open-ocean bacterial communities with organic carbon, nitrogen and phosphorus, and that phytoplankton exudate serve a full-fledged meal for specific members of the accompanying bacterial community in the nutrient-poor eastern Mediterranean.

ecology↗

bioRxiv2021

Seasonal dynamics of phytoplankton and bacterioplankton at the ultra-oligotrophic southeastern Mediterranean Sea

The Eastern Mediterranean Sea (EMS) is a poorly studied ultra-oligotrophic marine environment, dominated by small-size phyto- and bacterioplankton. Here, we describe the dynamics of a single annual cycle (2018-19) of phyto- and bacterioplankton (abundances, pigments and productivity) in relation to the physical and chemical conditions in the photic water column at an offshore EMS site (Station THEMO-2, [~]1,500m depth, 50km offshore). We show that phytoplankton biomass (as chlorophyll a), primary and bacterial productivity differed between the mixed winter (January-April) and the thermally stratified (May-December) periods. Prochlorococcus and Synechococcus numerically dominated the picophytoplankton populations, with each clade revealing different temporal and depth changes indicative to them, while pico-eukaryotes (primarily haptophytes) were less abundant, yet likely contributed significant biomass. Estimated primary productivity ([~]32 gC m-2 y-1) was lower compared with other well-studied oligotrophic locations, including the north Atlantic and Pacific (BATS and HOT observatories), the western Mediterranean (DYFAMED observatory) and the Red Sea, and was on-par with the ultra-oligotrophic South Pacific Gyre. In contrast, integrated bacterial production ([~]11 gC m-2 y-1) was similar to other oligotrophic locations. Phytoplankton seasonal dynamics were similar to those at BATS and the Red Sea, suggesting an observable effect of winter mixing in this ultra-oligotrophic location. These results highlight the ultra-oligotrophic conditions in the EMS and provide, for the first time in this region, a full-year baseline and context to ocean observatories in the region. HighlightsO_LIBacterioplankton dynamics were assessed monthly in the Eastern Mediterranean Sea C_LIO_LISmall-sized picophytoplankton numerically dominated the phytoplankton community C_LIO_LISeasonal phytoplankton dynamics are similar to BATS and Red Sea, but not to HOT C_LIO_LIAnnual primary productivity is among the lowest in the worlds oceans C_LIO_LIBacterial to primary production ratio is higher than most oligotrophic seas C_LI

microbiology↗

bioRxiv2020

Particle-associated and free-living bacterial communities in an oligotrophic sea are affected by different environmental and anthropogenic factors

In the oceans and seas, environmental conditions change over multiple temporal and spatial scales. Here, we ask what factors affect the bacterial community structure across time, depth and size fraction during six seasonal cruises (two years) in the ultra-oligotrophic Eastern Mediterranean Sea. The bacterial community varied most between size fractions (free-living vs particle-associated), followed by depth and finally season. The free-living (FL) community was taxonomically richer and more stable than the particle-associated (PA) one, which was characterized by recurrent "blooms" of heterotrophic bacteria such as Alteromonas and Ralstonia. The heterotrophic FL and PA communities were also correlated with different environmental parameters: depth and phytoplankton correlated with the FL population, whereas PA bacteria were correlated primarily with season. A significant part of the variability in community structure could not, however, be explained by the measured environmental parameters. The metabolic potential of the PA community, predicted from 16S amplicon data, was enriched in pathways associated with the degradation and utilization of biological macromolecules, as well as plastics, other petroleum products and herbicides. The FL community was enriched in pathways for the metabolism of inositol phosphate, a potential phosphorus source, and of polycyclic aromatic hydrocarbons. Originality - Significance StatementMarine microbial populations are complex and dynamic, and the environmental drivers of the structure and function of these communities are mostly unclear. Specifically, marine microbial communities change over time, over depth and between particle-associated and free-living size fractions, yet the relative importance of each of these axes of variability is unclear. Our results highlight fundamentally different population dynamics between free-living and particle-associated marine bacteria: free living populations were more similar between seasons, whereas particle-associated populations were highly variable and exhibited "blooms" of specific clades of heterotrophic bacteria. We also suggest that the environmental conditions often measured as part of oceanographic cruises are not enough to explain most of the variability in microbial population structure. We speculate that organismal interactions and the presence of anthropogenic pollution may be also be important yet under-sampled drivers of oligotrophic marine microbial communities.

ecology↗

bioRxiv2020

Microbial communities in an ultra-oligotrophic sea are more affected by season than by distancefrom shore

Marine microbial communities vary seasonally and spatially, but these two factors are rarely addressed together. We studied temporal and spatial patterns of the microbial community structure and activity along a coast to offshore transect from the Israeli coast of the Eastern Mediterranean Sea (EMS) over six cruises, in three seasons of two consecutive years. The ultra-oligotrophic status of the South Eastern Mediterranean Sea was reflected in the microbial community composition that was dominated by oligotrophic microbial groups such as SAR11 throughout the year, even at the most coastal station sampled. Seasons affected microbial communities much more than distance from shore explaining about half of the observed variability in the microbial community, compared to only about 6% that was explained by station. However, the most coastal site differed significantly in community structure and activity from the three further offshore stations in early winter and summer, but not in spring. Our data on the microbial community composition and its seasonality from a transect into the South Eastern Levantine basin support the notion that the EMS behaves similar to open gyres rather than an inland sea.

ecology↗

bioRxiv2019

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Every living cell is composed of macromolecules such as proteins, DNA, RNA and pigments. The ratio between these macromolecular pools depends on the allocation of resources within the organism to different physiological requirements, and in turn affects biogeochemical cycles of elements such as carbon, nitrogen and phosphorus. Here, we present detailed measurements of the macromolecular composition of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, as it grows and declines due to nitrogen starvation in laboratory batch cultures. As cells reached stationary stage and declined, protein per cell decreased by [~]30% whereas RNA per cell and pigments per cell decreased by [~]75%. The decline stage was associated with the appearance of chlorotic cells which had higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-chlorophyll-like pigments emerged, which were not observed during exponential growth. These divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern Mediterranean. Around >80% of the carbon fixed by Prochlorococcus MIT9312 (but not of a different strain, NATL2A) was released into the growth media as dissolved organic carbon under these laboratory conditions. Variations in RNA/protein indicate that, broadly defined, the macromolecular composition of Prochlorococcus MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, possibly due to the significant investment in photosynthetic machinery of phototrophs.

microbiology↗

bioRxiv2019

Prochlorococcus rely on microbial interactions rather than on chlorotic resting stages to survive long-term stress

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 NanoSIMS. However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not re-grow under axenic conditions when transferred to new media. Nevertheless, co-cultures 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. ImportanceThe ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions as is 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 impactful marine cyanobacterium. Instead, Prochlorococcus rely 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.

microbiology↗