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1. A Ubiquitously Conserved Cyanobacterial Protein Phosphatase Essential for High Light Tolerance in a Fast-Growing Cyanobacterium

   https://doi.org/10.1128/spectrum.01008-22  

   Walker, Patricia L. ; Pakrasi, Himadri B. ( August 2022 , Microbiology Spectrum)

   Youssef, Noha H. (Ed.)

   ABSTRACT Synechococcus elongatus UTEX 2973, the fastest-growing cyanobacterial strain known, optimally grows under extreme high light (HL) intensities of 1,500–2,500 μmol photons m −2 s −1 , which is lethal to most other photosynthetic microbes. We leveraged the few genetic differences between Synechococcus 2973 and the HL sensitive strain Synechococcus elongatus PCC 7942 to unravel factors essential for the high light tolerance. We identified a novel protein in Synechococcus 2973 that we have termed HltA for H igh l ight t olerance protein A . Using bioinformatic tools, we determined that HltA contains a functional PP2C-type protein phosphatase domain. Phylogenetic analysis showed that the PP2C domain belongs to the bacterial-specific Group II family and is closely related to the environmental stress response phosphatase RsbU. Additionally, we showed that unlike any previously described phosphatases, HltA contains a single N-terminal regulatory GAF domain. We found hltA to be ubiquitous throughout cyanobacteria, indicative of its potentially important role in the photosynthetic lifestyle of these oxygenic phototrophs. Mutations in the hltA gene resulted in severe defects specific to high light growth. These results provide evidence that hltA is a key factor in the tolerance of Synechococcus 2973 to high light and will open new insightsmore »into the mechanisms of cyanobacterial light stress response. IMPORTANCE Cyanobacteria are a diverse group of photosynthetic prokaryotes. The cyanobacterium Synechococcus 2973 is a high light tolerant strain with industrial promise due to its fast growth under high light conditions and the availability of genetic modification tools. Currently, little is known about the high light tolerance mechanisms of Synechococcus 2973, and there are many unknowns overall regarding high light tolerance of cyanobacteria. In this study, a comparative genomic analysis of Synechococcus 2973 identified a single nucleotide polymorphism in a locus encoding a serine phosphatase as a key factor for high light tolerance. This novel GAF-containing phosphatase was found to be the sole Group II metal-dependent protein phosphatase that is evolutionarily conserved throughout cyanobacteria. These results shed new light on the light response mechanisms of Synechococcus 2973, improving our understanding of environmental stress response. Additionally, this work will help facilitate the development of Synechococcus 2973 as an industrially useful organism.« less
2. Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals

   https://doi.org/10.1128/AEM.03175-20  

   Hoadley, Kenneth D. ; Hamilton, Maria ; Poirier, Camille L. ; Choi, Chang Jae ; Yung, Cheuk-Man ; Worden, Alexandra Z. ( April 2021 , Applied and Environmental Microbiology)

   Johnson, Karyn N. (Ed.)

   ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction inmore »heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down.« less
3. Prochlorococcus Exudate Stimulates Heterotrophic Bacterial Competition with Rival Phytoplankton for Available Nitrogen

   https://doi.org/10.1128/mbio.02571-21  

   Calfee, Benjamin C. ; Glasgo, Liz D. ; Zinser, Erik R. ( February 2022 , mBio)

   Martiny, Jennifer B. (Ed.)

   ABSTRACT The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study, we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and cocultures when nutrients were replete. However, in nitrogen-limited medium, Prochlorococcus outgrew Synechococcus but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen but only if stimulated by the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus inmore »nutrient-limited regions of the ocean. IMPORTANCE In nutrient-poor habitats, competition for limited resources is thought to select for organisms with an enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus , the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study, the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus , was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen and the presence of heterotrophic bacteria. The results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotroph’s ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups and how these interactions likely contribute to the success of the most abundant photosynthetic microorganism.« less
4. Cyanobacterial endobionts within a major marine planktonic calcifier (<i>Globigerina bulloides</i>, Foraminifera) revealed by 16S rRNA metabarcoding

   https://doi.org/10.5194/bg-14-901-2017  

   Bird, Clare ; Darling, Kate F. ; Russell, Ann D. ; Davis, Catherine V. ; Fehrenbacher, Jennifer ; Free, Andrew ; Wyman, Michael ; Ngwenya, Bryne T. ( January 2017 , Biogeosciences)

   Abstract. We investigated the possibility of bacterial symbiosis in Globigerina bulloides, a palaeoceanographically important, planktonic foraminifer. This marine protist is commonly used in micropalaeontological investigations of climatically sensitive subpolar and temperate water masses as well as wind-driven upwelling regions of the world's oceans. G. bulloides is unusual because it lacks the protist algal symbionts that are often found in other spinose species. In addition, it has a large offset in its stable carbon and oxygen isotopic compositions compared to other planktonic foraminifer species, and also that predicted from seawater equilibrium. This is suggestive of novel differences in ecology and life history of G. bulloides, making it a good candidate for investigating the potential for bacterial symbiosis as a contributory factor influencing shell calcification. Such information is essential to evaluate fully the potential response of G. bulloides to ocean acidification and climate change. To investigate possible ecological interactions between G. bulloides and marine bacteria, 18S rRNA gene sequencing, fluorescence microscopy, 16S rRNA gene metabarcoding and transmission electron microscopy (TEM) were performed on individual specimens of G. bulloides (type IId) collected from two locations in the California Current. Intracellular DNA extracted from five G. bulloides specimens was subjected to 16S rRNA gene metabarcoding and,more »remarkably, 37–87% of all 16S rRNA gene sequences recovered were assigned to operational taxonomic units (OTUs) from the picocyanobacterium Synechococcus. This finding was supported by TEM observations of intact Synechococcus cells in both the cytoplasm and vacuoles of G. bulloides. Their concentrations were up to 4 orders of magnitude greater inside the foraminifera than those reported for the California Current water column and approximately 5% of the intracellular Synechococcus cells observed were undergoing cell division. This suggests that Synechococcus is an endobiont of G. bulloides type IId, which is the first report of a bacterial endobiont in the planktonic foraminifera. We consider the potential roles of Synechococcus and G. bulloides within the relationship and the need to determine how widespread the association is within the widely distributed G. bulloides morphospecies. The possible influence of Synechococcus respiration on G. bulloides shell geochemistry is also explored.

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5. Interplay between differentially expressed enzymes contributes to light color acclimation in marine Synechococcus

   https://doi.org/10.1073/pnas.1810491116  

   Sanfilippo, Joseph E. ; Nguyen, Adam A. ; Garczarek, Laurence ; Karty, Jonathan A. ; Pokhrel, Suman ; Strnat, Johann A. ; Partensky, Frédéric ; Schluchter, Wendy M. ; Kehoe, David M. ( March 2019 , Proceedings of the National Academy of Sciences)

   MarineSynechococcus, a globally important group of cyanobacteria, thrives in various light niches in part due to its varied photosynthetic light-harvesting pigments. ManySynechococcusstrains use a process known as chromatic acclimation to optimize the ratio of two chromophores, green-light–absorbing phycoerythrobilin (PEB) and blue-light–absorbing phycourobilin (PUB), within their light-harvesting complexes. A full mechanistic understanding of howSynechococcuscells tune their PEB to PUB ratio during chromatic acclimation has not yet been obtained. Here, we show that interplay between two enzymes named MpeY and MpeZ controls differential PEB and PUB covalent attachment to the same cysteine residue. MpeY attaches PEB to the light-harvesting protein MpeA in green light, while MpeZ attaches PUB to MpeA in blue light. We demonstrate that the ratio ofmpeYtompeZmRNA determines if PEB or PUB is attached. Additionally, strains encoding only MpeY or MpeZ do not acclimate. Examination of strains ofSynechococcusisolated from across the globe indicates that the interplay between MpeY and MpeZ uncovered here is a critical feature of chromatic acclimation for marineSynechococcusworldwide.