Physiology and molecular biology of aquatic cyanobacteria

© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 5 (2014): 359, doi:10.3389/fmicb.2014.00359.Cyanobacteria thrive in every illuminated aquatic environment known, contributing at least 25% of primary productivity worldwide. Given their importance in carbon and nutrient cycles, cyanobacteria are essential geochemical agents that have shaped the composition of the Earth's crust, oceans and atmosphere for billions of years. The high diversity of cyanobacteria is reflected in the panoply of unique physiological adaptations across the phylum, including different strategies to optimize light harvesting or sustain nitrogen fixation, but also different lifestyles like psychrotrophy, and oligotrophy. Some cyanobacteria produce secondary metabolites of cryptic function, many of which are toxic to eukaryotes. Consequently, bloom-forming toxic cyanobacteria are global hazards that are of increasing concern in surface waters affected by anthropogenic nutrient loads and climate change

Distribution and expression of the cyanate acquisition potential among cyanobacterial populations in oligotrophic marine waters

Author Posting. © Association for the Sciences of Limnology and Oceanography, 2013. This article is posted here by permission of Association for the Sciences of Limnology and Oceanography for personal use, not for redistribution. The definitive version was published in Limnology and Oceanography 58 (2013): 1959-1971, doi:10.4319/lo.2013.58.6.1959.We assessed the significance of cyanate utilization in marine primary productivity from the distribution of a dedicated transporter (encoded by cynABD) in different ocean environments. Several lines of evidence indicate that the cyanate utilization potential is associated mainly with surface populations of Prochlorococcus. Spatial and temporal dimensions of cynA, cynS, and ntcA expression by picocyanobacteria in the northern Red Sea supported our previous finding that cynA transcripts accumulate under more stringent N-limiting conditions. At the same time, cyanate utilization appeared to be more complex than suggested in our earlier publication, as we showed that picocyanobacteria also express their cyanate utilization potential under conditions where labile organic N compounds, such as urea, accumulate. These include N-sufficient transient conditions that result from nutrient upwelling during early mixing events in autumn as well as during spring bloom conditions that follow deep mixing events. Our finding that cynA occurrence is common in diverse marine environments suggests that cyanate utilization may be of a more fundamental importance to picophytoplankton productivity than previously considered.Financial support for experimental work was provided by Israel Science Foundation grant 135/05; DNA sequencing, phylogenetic analyses, data processing, and manuscript preparation were supported by the National Science Foundation grant 1155566 in Chemical Oceanography

Characterization of cyanate metabolism in marine Synechococcus and Prochlorococcus spp.

Author Posting. © The Author(s), 2010. This is the author's version of the work. It is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 77 (2011): 291-301, doi:10.1128/AEM.01272-10.Cyanobacteria of the genera Synechococcus and Prochlorococcus are the most abundant photosynthetic organism on Earth occupying a key position at the base of marine food webs. The cynS gene that encodes cyanase was identified among bacterial, fungi and plant sequences in public databases and the gene was particularly prevalent among cyanobacteria, including numerous Prochlorococcus and Synechococcus strains. Phylogenetic analysis of cynS sequences retrieved from the Global Ocean Survey database identified >60% as belonging to unicellular marine cyanobacteria, suggesting an important role for cyanase in their nitrogen metabolism. Here we showed that marine cyanobacteria have a functionally active cyanase, the transcriptional regulation of which varies among strains and reflects the genomic context of cynS. In Prochlorococcus sp. MED4, cynS was presumably transcribed as part of the cynABDS operon, implying cyanase involvement in cyanate utilization. In Synechococcus sp. WH8102, expression was not related to nitrogen stress responses and here cyanase presumably serves in the detoxification of cyanate resulting from intracellular urea and/or carbamoyl phosphate decomposition. Lastly, we report on a cyanase activity encoded by cynH, a novel gene found in marine cyanobacteria only. The presence of dual cyanase genes in genomes of seven marine Synechococcus strains and their respective roles in nitrogen metabolism remain to be clarified.The Niedersachsen State Fund at the Hebrew University, the Israel Science Foundation (grant 135/05) and the NATO Science for Peace program (grant SfP 98216) all provided financial support

Functional Plasticity in Oyster Gut Microbiomes along a Eutrophication Gradient in an Urbanized Estuary

Background Oysters in coastal environments are subject to fluctuating environmental conditions that may impact the ecosystem services they provide. Oyster-associated microbiomes are responsible for some of these services, particularly nutrient cycling in benthic habitats. The effects of climate change on host-associated microbiome composition are well-known, but functional changes and how they may impact host physiology and ecosystem functioning are poorly characterized. We investigated how environmental parameters affect oyster-associated microbial community structure and function along a trophic gradient in Narragansett Bay, Rhode Island, USA. Adult eastern oyster, Crassostrea virginica, gut and seawater samples were collected at 5 sites along this estuarine nutrient gradient in August 2017. Samples were analyzed by 16S rRNA gene sequencing to characterize bacterial community structures and metatranscriptomes were sequenced to determine oyster gut microbiome responses to local environments. Results There were significant differences in bacterial community structure between the eastern oyster gut and water samples, suggesting selection of certain taxa by the oyster host. Increasing salinity, pH, and dissolved oxygen, and decreasing nitrate, nitrite and phosphate concentrations were observed along the North to South gradient. Transcriptionally active bacterial taxa were similar for the different sites, but expression of oyster-associated microbial genes involved in nutrient (nitrogen and phosphorus) cycling varied throughout the Bay, reflecting the local nutrient regimes and prevailing environmental conditions. Conclusions The observed shifts in microbial community composition and function inform how estuarine conditions affect host-associated microbiomes and their ecosystem services. As the effects of estuarine acidification are expected to increase due to the combined effects of eutrophication, coastal pollution, and climate change, it is important to determine relationships between host health, microbial community structure, and environmental conditions in benthic communities

Genome reconstructions indicate the partitioning of ecological functions inside a phytoplankton bloom in the Amundsen Sea, Antarctica

© The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 6 (2015): 1090, doi:10.3389/fmicb.2015.01090.Antarctica polynyas support intense phytoplankton blooms, impacting their environment by a substantial depletion of inorganic carbon and nutrients. These blooms are dominated by the colony-forming haptophyte Phaeocystis antarctica and they are accompanied by a distinct bacterial population. Yet, the ecological role these bacteria may play in P. antarctica blooms awaits elucidation of their functional gene pool and of the geochemical activities they support. Here, we report on a metagenome (~160 million reads) analysis of the microbial community associated with a P. antarctica bloom event in the Amundsen Sea polynya (West Antarctica). Genomes of the most abundant Bacteroidetes and Proteobacteria populations have been reconstructed and a network analysis indicates a strong functional partitioning of these bacterial taxa. Three of them (SAR92, and members of the Oceanospirillaceae and Cryomorphaceae) are found in close association with P. antarctica colonies. Distinct features of their carbohydrate, nitrogen, sulfur and iron metabolisms may serve to support mutualistic relationships with P. antarctica. The SAR92 genome indicates a specialization in the degradation of fatty acids and dimethylsulfoniopropionate (compounds released by P. antarctica) into dimethyl sulfide, an aerosol precursor. The Oceanospirillaceae genome carries genes that may enhance algal physiology (cobalamin synthesis). Finally, the Cryomorphaceae genome is enriched in genes that function in cell or colony invasion. A novel pico-eukaryote, Micromonas related genome (19.6 Mb, ~94% completion) was also recovered. It contains the gene for an anti-freeze protein, which is lacking in Micromonas at lower latitudes. These draft genomes are representative for abundant microbial taxa across the Southern Ocean surface.This work was performed with financial support from NSF Antarctic Sciences awards ANT-1142095 to AP

Diversity of Synechococcus at the Martha\u27s Vineyard Coastal Observatory: Insights from Culture Isolations, Clone Libraries, and Flow Cytometry

The cyanobacterium Synechococcus is a ubiquitous, important phytoplankter across the world’s oceans. A high degree of genetic diversity exists within the marine group, which likely contributes to its global success. Over 20 clades with different distribution patterns have been identified. However, we do not fully understand the environmental factors that control clade distributions. These factors are likely to change seasonally, especially in dynamic coastal systems. To investigate how coastal Synechococcus assemblages change temporally, we assessed the diversity of Synechococcus at the Martha’s Vineyard Coastal Observatory (MVCO) over three annual cycles with culture-dependent and independent approaches. We further investigated the abundance of both phycoerythrin (PE)-containing and phycocyanin (PC)-only Synechococcus with a flow cytometric setup that distinguishes PC-only Synechococcus from picoeukaryotes. We found that the Synechococcus assemblage at MVCO is diverse (13 different clades identified), but dominated by clade I representatives. Many clades were only isolated during late summer and fall, suggesting more favorable conditions for isolation at this time. PC-only strains from four different clades were isolated, but these cells were only detected by flow cytometry in a few samples over the time series, suggesting they are rare at this site. Within clade I, we identified four distinct subclades. The relative abundances of each subclade varied over the seasonal cycle, and the high Synechococcus cell concentration at MVCO may be maintained by the diversity found within this clade. This study highlights the need to understand how temporal aspects of the environment affect Synechococcus community structure and cell abundance

Identification, enumeration and diversity of nitrifying planktonic archaea and bacteria in trophic end members of the Laurentian Great Lakes

Oligotrophic Lake Superior and mesotrophic Lake Erie are trophic end members of the hydrologically connected Laurentian Great Lakes system, and as such exhibit different profiles of dissolved nitrogen species. Nitrification in Lake Superior has led to increasing nitrate concentrations over the past century, as opposed to Erie, where nitrate inventories have declined due to denitrification. In this study, we examined the abundance and diversity of nitrifying microbes involved in the oxidation of ammonia to nitrite, and nitrite to nitrate. By in situ hybridization methods, we enumerated the major planktonic ammonia oxidizing bacteria (AOB) and archaea (AOA) during a July 2011 cruise from Lake Superior to Lake Erie. In Lake Superior, AOA dominated compared to AOB, typically exceeding 5 × 103 mL-1, whereas in Erie, AOB were more abundant than AOA. These data parallel prior work on Lake Superior and Lake Erie sediments, in which AOA are far more abundant in Superior, but AOB dominate in Erie. The lakes were sampled during stratification, and AOA and AOB were largely restricted to the hypolimnion, consistent with the observation that ammonia oxidizers are photoinhibited in surface waters. In Lakes Superior and Erie, we also detected nitrite oxidizing bacteria (NOB) in a pattern paralleling AOA/AOB abundance. Phylogenetic analysis of archaeal 16S rRNA revealed that the planktonic archaea of Lake Superior are members of the ammonia oxidizing Group I.1a Thaumarchaeota most closely related to Nitrosoarchaeum limnia. These AOA are distinct from the Group I.1a AOA in Lake Superior sediments. The major AOB of Lake Erie form a subcluster within the genus Nitrosospira

Ecological functions of uncultured microorganisms in the cobalt-rich ferromanganese crust of a seamount in the central Pacific are elucidated by fosmid sequencing

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Acta Oceanologica Sinica 34 (2015):92-113, doi:10.1007/s13131-015-0650-7.Cobalt-rich ferromanganese is an important seafloor mineral and is abundantly present in the seamount crusts. Such crusts form potential hotspots for biogeochemical activity and microbial diversity, yet our understanding of their microbial communities is lacking. In this study, we used a cultivation-independent approach to recover genomic information and derive ecological functions of the microbes in a sediment sample collected from the cobalt-rich ferromanganese crust of a seamount region in the central Pacific. A total of 78 distinct clones were obtained by fosmid library screening with a 16S rRNA based PCR method. Proteobacteria and MGI Thaumarchaeota dominated the bacterial and archaeal 16S rRNA gene sequence results in the microbial community. Nine fosmid clones were sequenced and annotated. Numerous genes encoding proteins involved in metabolic functions and heavy metal resistance were identified, suggesting alternative metabolic pathways and stress responses that are essential for microbial survival in the cobalt-rich ferromanganese crust. In addition, genes that participate in the synthesis of organic acids and exoploymers were discovered. Reconstruction of the metabolic pathways revealed that the nitrogen cycle is an important biogeochemical process in the cobalt-rich ferromanganese crust. In addition, horizontal gene transfer (HGT) events have been observed, and most of them came from bacteria, with some occurring in archaea and plants. Clone W4-93a, belonging to MGI Thaumarchaeota, contained a region of gene synteny. Comparative analyses suggested that a high frequency of HGT events as well as genomic divergence play important roles in the microbial adaption to the deep-sea environment.China Ocean Mineral Resources R & D Association (COMRA) Special Foundation (No. DY125-15-R-03 and DY125-13-E-01); the National Natural Science Foundation of China (No. 41276173); the Zhejiang Provincial Natural Science Foundation of China (No. LQ13D060002) and the Scientific Research Fund of the Second Institute of Oceanography, SOA (No. JT1305).2016-04-1

Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation

Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 112 (2015): 9944-9949, doi:10.1073/pnas.1509448112.Marine Synechococcus are some of the most diverse and ubiquitous phytoplankton, and iron (Fe) is an essential micronutrient that limits productivity in many parts of the ocean. To investigate how coastal and oceanic Atlantic Synechococcus strains acclimate to Fe availability, we compared the growth, photophysiology, and quantitative proteomics of two Synechococcus strains from different Fe regimes. Synechococcus strain WH8102, from a region in the southern Sargasso Sea that receives substantial dust deposition, showed impaired growth and photophysiology as Fe declined, yet utilized few acclimation responses. Coastal WH8020, from the dynamic, seasonally variable New England shelf, displayed a multi-tiered, hierarchical cascade of acclimation responses with different Fe thresholds. The multi-tiered response included changes in Fe acquisition, storage, and photosynthetic proteins, substitution of flavodoxin for ferredoxin, and modified photophysiology, all while maintaining remarkably stable growth rates over a range of Fe concentrations. Modulation of two distinct ferric uptake regulator (Fur) proteins that coincided with the multi-tiered proteome response was found, implying the coastal strain has different regulatory threshold responses to low Fe availability. Low nitrogen (N) and phosphorus (P) availability in the open ocean may favor the loss of Fe response genes when Fe availability is consistent over time, whereas these genes are retained in dynamic environments where Fe availability fluctuates and N and P are more abundant.This work was supported by a National Science Foundation Postdoctoral Research Fellowship in Biology to K.R.M.M. (NSF 1103575), National Science Foundation Oceanography grants OCE-1220484, OCE-0928414, OCE-1233261, OCE- 1155566, OCE-1131387, and OCE-0926092, as well as Gordon and Betty Moore Foundation grants 3782 and 3934