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Hogle, SL, Dupont CL, Hopkinson BM, King AL, Buck KN, Roe KL, Stuart RK, Allen AE, Mann EL, Johnson ZI, Barbeau KA.  2018.  Pervasive iron limitation at subsurface chlorophyll maxima of the California Current. Proceedings of the National Academy of Sciences of the United States of America. 115:13300-13305.   10.1073/pnas.1813192115   AbstractWebsite

Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO3). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwelling zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

Hogle, SL, Thrash JC, Dupont CL, Barbeau KA.  2016.  Trace metal acquisition by marine heterotrophic bacterioplankton with contrasting trophic strategies. Applied and Environmental Microbiology. 82:1613-1624.   10.1128/aem.03128-15   AbstractWebsite

Heterotrophic bacteria in the SAR11 and Roseobacter lineages shape the marine carbon, nitrogen, phosphorous, and sulfur cycles, yet they do so having adopted divergent ecological strategies. Currently, it is unknown whether these globally significant groups partition into specific niches with respect to micronutrients (e.g., trace metals) and how that may affect marine trace metal cycling. Here, we used comparative genomics to identify diverse iron, cobalt, nickel, copper, and zinc uptake capabilities in SAR11 and Roseobacter genomes and uncover surprising unevenness within and between lineages. The strongest predictors for the extent of the metal uptake gene content are the total number of transporters per genome, genome size, total metal transporters, and GC content, but numerous exceptions exist in both groups. Taken together, our results suggest that SAR11 have strongly minimized their trace metal uptake versatility, with high-affinity zinc uptake being a unique exception. The larger Roseobacter genomes have greater trace metal uptake versatility on average, but they also appear to have greater plasticity, resulting in phylogenetically similar genomes having largely different capabilities. Ultimately, phylogeny is predictive of the diversity and extent of 20 to 33% of all metal uptake systems, suggesting that specialization in metal utilization mostly occurred independently from overall lineage diversification in both SAR11 and Roseobacter. We interpret these results as reflecting relatively recent trace metal niche partitioning in both lineages, suggesting that concentrations and chemical forms of metals in the marine environment are important factors shaping the gene content of marine heterotrophic Alphaproteobacteria of the SAR11 and Roseobacter lineages.

Dupont, CL, McCrow JP, Valas R, Moustafa A, Walworth N, Goodenough U, Roth R, Hogle SL, Bai J, Johnson ZI, Mann E, Palenik B, Barbeau KA, Craig Venter J, Allen AE.  2015.  Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J. 9:1076-1092.: International Society for Microbial Ecology   10.1038/ismej.2014.198   Abstract

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-[mu]m size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.

Dupont, CL, Buck KN, Palenik B, Barbeau K.  2010.  Nickel utilization in phytoplankton assemblages from contrasting oceanic regimes. Deep-Sea Research Part I-Oceanographic Research Papers. 57:553-566.   10.1016/j.dsr.2009.12.014   AbstractWebsite

In most oceanic environments, dissolved nickel (Ni) concentrations are drawn clown in surface waters with increasing concentrations at depth, implying a role for biology in the geochemical distribution of Ni Studies with phytoplankton isolates from the surface ocean have established the biochemical roles of Ni in the assimilation of urea and oxidative defense To determine if these requirements are relevant in natural marine planktonic assemblages, bottle-based fertilization experiments were used to test the effects of low-level additions of Ni. urea, or both Ni and urea to surface waters at several locations offshore of Peru and California, as well as in the Gulf of California Urea and Ni(+) urea additions consistently promoted phytoplankton growth relative to control and +Ni treatments, except in a coastal upwelling site and Peruvian water. No effect was observed in the upwelling site, but in Peruvian waters urea additions resulted in increased phytoplankton pigments and phosphate drawdown only when Ni was added concurrently, suggesting a biochemically dependent Ni-urea colimitation In the Gulf of California, Ni additions without urea resulted in increased abundances of cyanobacteria, picoeukaryotes, and the corresponding pigments As urea additions showed the overall phytoplankton community was also urea-limited, it appears that the cyanobactena and potentially the picoeukaryotes were colimited by Ni and urea in a biochemically independent fashion. In parallel, radiotracer-based uptake experiments were used to study the kinetics and spatial variation of biological Ni assimilation. In these experiments, the added radiotracer rarely equilibrated with the natural Ni present, precluding estimates a determination of in situ Ni uptake rates and suggesting that much of the natural Ni was not bioavailable. The lack of equilibration likely did not preclude the measurement of community Ni uptake kinetics, nor the comparison of measured rates between locations The highest V(max)K(p)(-1) values, which reflect a competitive advantage in Ni acquisition at low concentrations, were observed in stratified nitrogen-deplete communities, potentially linking Ni and nitrogen biogeochemistry in a manner consistent with the biochemical utilization of Ni. Overall, uptake rates were higher in the euphotic rather than non-euphotic zone communities, directly reconciling the nutrient-like depth profile of Ni The Ni uptake rates observed at the nitrate-replete Fe-deplete Peru stations were an order of magnitude lower than the other sites This result agrees with calculations suggesting that saturation of the cell surface with Ni and iron (Fe) transporters may limit uptake rates in low Fe waters. (C) 2010 Elsevier Ltd. All rights reserved

Dupont, CL, Barbeau K, Palenik B.  2008.  Ni uptake and limitation in marine Synechococcus strains. Applied and Environmental Microbiology. 74:23-31.   10.1128/aem.01007-07   AbstractWebsite

Ni accumulation and utilization were studied in two strains of marine Synechococcus, isolated from both coastal (CC9311; clade I) and open-ocean (WTH8102; clade III) environments, for which complete genome sequences are available. Both strains have genes encoding an Ni-containing urease and when grown on urea without Ni become Ni-N colimited. The Ni requirements of these strains also depend upon the genomic complement of genes encoding superoxide dismutase (SOD). WH8102, with a gene encoding only an Ni-SOD, has a novel obligate requirement for Ni, regardless of the N source. Reduced SOD activity in Ni-depleted cultures of VM8102 supports the link of this strain's Ni requirement to Ni-SOD. The genome of CC9311 contains a gene for a Cu/Zn-SOD in addition to a predicted pair of Ni-SODs, yet this strain cannot grow without Ni on NO3- and can grow only slowly on NH4+ without Ni, implying that the Cu/Zn-SOD cannot completely replace Ni-SOD in marine cyanobacteria. CC9311 does have a greater tolerance for Ni starvation. Both strains increase their Ni uptake capabilities and actively bioconcentrate Ni in response to decreasing extracellular and intracellular Ni. The changes in Ni uptake rates were more pronounced in WH8102 than in CC9311 and for growth on urea or nitrate than for growth on ammonia. These results, combined with an analysis of fully sequenced marine cyanobacterial genomes, suggest that the growth of many marine Synechococcus and all Prochlorococcus strains is dependent upon Ni.