Post Anton F.

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Needles in the blue sea : sub-species specificity in targeted protein biomarker analyses within the vast oceanic microbial metaproteome

( 2015-03-27) Saito, Mak A. ; Dorsk, Alexander ; Post, Anton F. ; McIlvin, Matthew R. ; Rappe, Michael S. ; DiTullio, Giacomo R. ; Moran, Dawn M.

Proteomics has great potential for studies of marine microbial biogeochemistry, yet high microbial diversity in many locales presents us with unique challenges. We addressed this challenge with a targeted metaproteomics workflow for NtcA and P-II, two nitrogen regulatory proteins, and demonstrated its application for cyanobacterial taxa within microbial samples from the Central Pacific Ocean. Using METATRYP, an open-source Python toolkit, we examined the number of shared (redundant) tryptic peptides in representative marine microbes, with the number of tryptic peptides shared between different species typically being 1% or less. The related cyanobacteria Prochlorococcus and Synechococcus shared an average of 4.8+1.9% of their tryptic peptides, while shared intraspecies peptides were higher, 13+15% shared peptides between 12 Prochlorococcus genomes. An NtcA peptide was found to target multiple cyanobacteria species, whereas a P-II peptide showed specificity to the high-light Prochlorococcus ecotype. Distributions of NtcA and P-II in the Central Pacific Ocean were similar except at the Equator likely due to differential nitrogen stress responses between Prochlorococcus and Synechococcus. The number of unique tryptic peptides coded for within three combined oceanic microbial metagenomes was estimated to be ~4x107, 1000-fold larger than an individual microbial proteome and 27-fold larger than the human proteome, yet still 20 orders of magnitude lower than the peptide diversity possible in all protein space, implying that peptide mapping algorithms should be able to withstand the added level of complexity in metaproteomic samples.
Distribution and expression of the cyanate acquisition potential among cyanobacterial populations in oligotrophic marine waters

(Association for the Sciences of Limnology and Oceanography, 2013-11) Kamennaya, Nina A. ; Post, Anton F.

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.
Characterization of cyanate metabolism in marine Synechococcus and Prochlorococcus spp.

( 2010-10-14) Kamennaya, Nina A. ; Post, Anton F.

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.
Microbial rhodopsins on leaf surfaces of terrestrial plants

( 2011-06-14) Atamna-Ismaeel, Nof ; Finkel, Omri M. ; Glaser, Fabian ; Sharon, Itai ; Schneider, Ron ; Post, Anton F. ; Spudich, John L. ; von Mering, Christian ; Vorholt, Julia A. ; Iluz, David ; Beja, Oded ; Belkin, Shimshon

The above-ground surfaces of terrestrial plants, the phyllosphere, comprise the main interface between the terrestrial biosphere and solar radiation. It is estimated to host up to 1026 microbial cells that may intercept part of the photon flux impinging on the leaves. Based on 454- pyrosequencing generated metagenome data, we report on the existence of diverse microbial rhodopsins in five distinct phyllospheres from tamarisk (Tamarix nilotica), soybean (Glycine max), Arabidopsis (Arabidopsis thaliana), clover (Trifolium repens) and rice (Oryza sativa). Our findings, for the first time describing microbial rhodopsins from non-aquatic habitats, point toward the potential coexistence of microbial rhodopsin-based phototrophy and plant chlorophyll-based photosynthesis, with the different pigments absorbing non-overlapping fractions of the light spectrum.
Physiology and molecular biology of aquatic cyanobacteria

(Frontiers Media, 2014-07-14) Bullerjahn, George S. ; Post, Anton F.

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.
ASPIRE : the Amundsen Sea Polynya International Research Expedition

(The Oceanography Society, 2012-09) Yager, Patricia L. ; Sherrell, Robert M. ; Stammerjohn, Sharon E. ; Alderkamp, Anne-Carlijn ; Schofield, Oscar M. E. ; Abrahamsen, E. Povl ; Arrigo, Kevin R. ; Bertilsson, Stefan ; Garay, D. Lollie ; Guerrero, Raul ; Lowry, Kate E. ; Moksnes, Per-Olav ; Ndungu, Kuria ; Post, Anton F. ; Randall-Goodwin, Evan ; Riemann, Lasse ; Severmann, Silke ; Thatje, Sven ; van Dijken, Gert L. ; Wilson, Stephanie

In search of an explanation for some of the greenest waters ever seen in coastal Antarctica and their possible link to some of the fastest melting glaciers and declining summer sea ice, the Amundsen Sea Polynya International Research Expedition (ASPIRE) challenged the capabilities of the US Antarctic Program and RVIB Nathaniel B. Palmer during Austral summer 2010–2011. We were well rewarded by both an extraordinary research platform and a truly remarkable oceanic setting. Here we provide further insights into the key questions that motivated our sampling approach during ASPIRE and present some preliminary findings, while highlighting the value of the Palmer for accomplishing complex, multifaceted oceanographic research in such a challenging environment.
Satellite remote sensing data can be used to model marine microbial metabolite turnover

(Nature Publishing Group, 2014-07-29) Larsen, Peter E. ; Scott, Nicole ; Post, Anton F. ; Field, Dawn ; Knight, Rob ; Hamada, Yuki ; Gilbert, Jack A.

Sampling ecosystems, even at a local scale, at the temporal and spatial resolution necessary to capture natural variability in microbial communities are prohibitively expensive. We extrapolated marine surface microbial community structure and metabolic potential from 72 16S rRNA amplicon and 8 metagenomic observations using remotely sensed environmental parameters to create a system-scale model of marine microbial metabolism for 5904 grid cells (49 km2) in the Western English Chanel, across 3 years of weekly averages. Thirteen environmental variables predicted the relative abundance of 24 bacterial Orders and 1715 unique enzyme-encoding genes that encode turnover of 2893 metabolites. The genes’ predicted relative abundance was highly correlated (Pearson Correlation 0.72, P-value <10−6) with their observed relative abundance in sequenced metagenomes. Predictions of the relative turnover (synthesis or consumption) of CO2 were significantly correlated with observed surface CO2 fugacity. The spatial and temporal variation in the predicted relative abundances of genes coding for cyanase, carbon monoxide and malate dehydrogenase were investigated along with the predicted inter-annual variation in relative consumption or production of ~3000 metabolites forming six significant temporal clusters. These spatiotemporal distributions could possibly be explained by the co-occurrence of anaerobic and aerobic metabolisms associated with localized plankton blooms or sediment resuspension, which facilitate the presence of anaerobic micro-niches. This predictive model provides a general framework for focusing future sampling and experimental design to relate biogeochemical turnover to microbial ecology.
Phyllosphere microbial communities of a salt-excreting desert tree : geographical location determines population structure

( 2011-09) Finkel, Omri M. ; Burch, Adrien Y. ; Lindow, Steven E. ; Post, Anton F. ; Belkin, Shimshon

The leaf surfaces of Tamarix, a salt secreting desert tree, harbor a diverse community of microbial epiphytes. This ecosystem presents a unique set of ecological characteristics and imposes a set of extreme stress conditions. The composition of the microbial community along ecological gradients was studied from analyses of microbial richness and diversity in the phyllosphere of three Tamarix species in the Mediterranean and Dead Sea regions in Israel, and in two locations in the USA. Over 200,000 sequences of the 16S-V6 and 18S-V9 hypervariable regions revealed a diverse community, with 788 bacterial and 64 eukaryotic genera, but only one archaeal genus. Both geographic location and tree species were determinants of microbial community structures, with the former being more dominant. Tree leaves of all three species in the Mediterranean region were dominated by Halomonas and Halobacteria, whereas trees from the Dead Sea area were dominated by Actinomycetales and Bacillales. Our findings demonstrate that microbial phyllosphere communities on different Tamarix species are highly similar in the same locale, whereas trees of the same species that grow in different climatic regions host distinct microbial communities.
The influence of light on nitrogen cycling and the primary nitrite maximum in a seasonally stratified sea

( 2011-07-08) Mackey, Katherine R. M. ; Bristow, Laura ; Parks, David R. ; Altabet, Mark A. ; Post, Anton F. ; Paytan, Adina

In the seasonally stratified Gulf of Aqaba Red Sea, both NO2- release by phytoplankton and NH4+ oxidation by nitrifying microbes contributed to the formation of a primary nitrite maximum (PNM) over different seasons and depths in the water column. In the winter and during the days immediately following spring stratification, NO2- formation was strongly correlated (R2=0.99) with decreasing irradiance and chlorophyll, suggesting that incomplete NO3- reduction by light limited phytoplankton was a major source of NO2-. However, as stratification progressed, NO2- continued to be generated below the euphotic depth by microbial NH4+ oxidation, likely due to differential photoinhibition of NH4+ and NO2- oxidizing populations. Natural abundance stable nitrogen isotope analyses revealed a decoupling of the δ15N and δ18O in the combined NO3- and NO2- pool, suggesting that assimilation and nitrification were co-occurring in surface waters. As stratification progressed, the δ15N of particulate N below the euphotic depth increased from -5‰ to up to +20‰. N uptake rates were also influenced by light; based on 15N tracer experiments, assimilation of NO3-, NO2-, and urea was more rapid in the light (434±24, 94±17, and 1194±48 nmol N L-1 day-1 respectively) than in the dark (58±14, 29±14, and 476±31 nmol N L-1 day-1 respectively). Dark NH4+ assimilation was 314±31 nmol N L-1 day-1, while light NH4+ assimilation was much faster, resulting in complete consumption of the 15N spike in less than 7 hour from spike addition. The overall rate of coupled urea mineralization and NH¬4+ oxidation (14.1±7.6 nmol N L-1 day-1) was similar to that of NH¬4+ oxidation alone (16.4±8.1 nmol N L-1 day-1), suggesting that for labile dissolved organic N compounds like urea, mineralization was not a rate limiting step for nitrification. Our results suggest that assimilation and nitrification compete for NH4+ and that N transformation rates throughout the water column are influenced by light over diel and seasonal cycles, allowing phytoplankton and nitrifying microbes to contribute jointly to PNM formation. We identify important factors that influence the N cycle throughout the year, including light intensity, substrate availability, and microbial community structure. These processes could be relevant to other regions worldwide where seasonal variability in mixing depth and stratification influence the contributions of phytoplankton and non-photosynthetic microbes to the N cycle.
Rapid and gradual modes of aerosol trace metal dissolution in seawater

(Frontiers Media, 2015-01-21) Mackey, Katherine R. M. ; Chien, Chia-Te ; Post, Anton F. ; Saito, Mak A. ; Paytan, Adina

Atmospheric deposition is a major source of trace metals in marine surface waters and supplies vital micronutrients to phytoplankton, yet measured aerosol trace metal solubility values are operationally defined, and there are relatively few multi-element studies on aerosol-metal solubility in seawater. Here we measure the solubility of aluminum (Al), cadmium (Cd), cobalt (Co), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), lead (Pb), and zinc (Zn) from natural aerosol samples in seawater over a 7 days period to (1) evaluate the role of extraction time in trace metal dissolution behavior and (2) explore how the individual dissolution patterns could influence biota. Dissolution behavior occurs over a continuum ranging from rapid dissolution, in which the majority of soluble metal dissolved immediately upon seawater exposure (Cd and Co in our samples), to gradual dissolution, where metals dissolved slowly over time (Zn, Mn, Cu, and Al in our samples). Additionally, dissolution affected by interactions with particles was observed in which a decline in soluble metal concentration over time occurred (Fe and Pb in our samples). Natural variability in aerosol chemistry between samples can cause metals to display different dissolution kinetics in different samples, and this was particularly evident for Ni, for which samples showed a broad range of dissolution rates. The elemental molar ratio of metals in the bulk aerosols was 23,189Fe: 22,651Al: 445Mn: 348Zn: 71Cu: 48Ni: 23Pb: 9Co: 1Cd, whereas the seawater soluble molar ratio after 7 days of leaching was 11Fe: 620Al: 205Mn: 240Zn: 20Cu: 14Ni: 9Pb: 2Co: 1Cd. The different kinetics and ratios of aerosol metal dissolution have implications for phytoplankton nutrition, and highlight the need for unified extraction protocols that simulate aerosol metal dissolution in the surface ocean.
Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria)

( 2011-08) Sukenik, Assaf ; Kaplan-Levy, Ruth N. ; Mark Welch, Jessica L. ; Post, Anton F.

Akinetes are dormancy cells commonly found among filamentous cyanobacteria, many of which are toxic and/or nuisance, bloom-forming species. Development of akinetes from vegetative cells is a process that involves morphological and biochemical modifications. Here we applied a single cell approach to quantify genome and ribosome content of akinetes and vegetative cells in Aphanizomenon ovalisporum (Cyanobacteria). Vegetative cells of A. ovalisporum were naturally polyploid and contained on average 8 genome copies per cell. However, the chromosomal content of akinetes increased up to 450 copies, with an average value of 119 genome copies per akinete, 15 fold higher that in vegetative cells. Based on fluorescence in situ hybridization with a probe targeting 16S rRNA and detection with confocal laser scanning microscopy we conclude that ribosomes accumulated in akinetes to a higher level than that found in vegetative cells. We further present evidence that this massive accumulation of nucleic acids in akinetes is likely supported by phosphate supplied from inorganic polyphosphate bodies that were abundantly present in vegetative cells, but notably absent from akinetes. These results are interpreted in the context of cellular investments for proliferation following long term dormancy, as the high nucleic acid content would provide the basis for extended survival, rapid resumption of metabolic activity and cell division upon germination.
Ecological functions of uncultured microorganisms in the cobalt-rich ferromanganese crust of a seamount in the central Pacific are elucidated by fosmid sequencing

( 2014-07) Huo, Yingyi ; Cheng, Hong ; Post, Anton F. ; Wang, Chunsheng ; Jiang, Xiawei ; Pan, Jie ; Wu, Min ; Xu, Xuewei

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.
Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya

(Frontiers Media, 2014-12-19) Delmont, Tom O. ; Hammar, Katherine M. ; Ducklow, Hugh W. ; Yager, Patricia L. ; Post, Anton F.

Rising temperatures and changing winds drive the expansion of the highly productive polynyas (open water areas surrounded by sea ice) abutting the Antarctic continent. Phytoplankton blooms in polynyas are often dominated by the haptophyte Phaeocystis antarctica, and they generate the organic carbon that enters the resident microbial food web. Yet, little is known about how Phaeocystis blooms shape bacterial community structures and carbon fluxes in these systems. We identified the bacterial communities that accompanied a Phaeocystis bloom in the Amundsen Sea polynya during the austral summers of 2007–2008 and 2010–2011. These communities are distinct from those determined for the Antarctic Circumpolar Current (ACC) and off the Palmer Peninsula. Diversity patterns for most microbial taxa in the Amundsen Sea depended on location (e.g., waters abutting the pack ice near the shelf break and at the edge of the Dotson glacier) and depth, reflecting different niche adaptations within the confines of this isolated ecosystem. Inside the polynya, P. antarctica coexisted with the bacterial taxa Polaribacter sensu lato, a cryptic Oceanospirillum, SAR92 and Pelagibacter. These taxa were dominated by a single oligotype (genotypes partitioned by Shannon entropy analysis) and together contributed up to 73% of the bacterial community. Size fractionation of the bacterial community [<3 μm (free-living bacteria) vs. >3 μm (particle-associated bacteria)] identified several taxa (especially SAR92) that were preferentially associated with Phaeocystis colonies, indicative of a distinct role in Phaeocystis bloom ecology. In contrast, particle-associated bacteria at 250 m depth were enriched in Colwellia and members of the Cryomorphaceae suggesting that they play important roles in the decay of Phaeocystis blooms.
Genome reconstructions indicate the partitioning of ecological functions inside a phytoplankton bloom in the Amundsen Sea, Antarctica

(Frontiers Media, 2015-10-26) Delmont, Tom O. ; Eren, A. Murat ; Vineis, Joseph H. ; Post, Anton F.

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.
Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation

( 2015-06-19) Mackey, Katherine R. M. ; Post, Anton F. ; McIlvin, Matthew R. ; Cutter, Gregory A. ; John, Seth G. ; Saito, Mak A.

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.

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