Life requires a wide variety of bioessential trace elements to act as structural components and reactive centers in metalloenzymes. These requirements differ between organisms and have evolved over ...geological time, likely guided in some part by environmental conditions. Until recently, most of what was understood regarding trace element concentrations in the Precambrian oceans was inferred by extrapolation, geochemical modeling, and/or genomic studies. However, in the past decade, the increasing availability of trace element and isotopic data for sedimentary rocks of all ages has yielded new, and potentially more direct, insights into secular changes in seawater composition – and ultimately the evolution of the marine biosphere. Compiled records of many bioessential trace elements (including Ni, Mo, P, Zn, Co, Cr, Se, and I) provide new insight into how trace element abundance in Earth's ancient oceans may have been linked to biological evolution. Several of these trace elements display redox-sensitive behavior, while others are redox-sensitive but not bioessential (e.g., Cr, U). Their temporal trends in sedimentary archives provide useful constraints on changes in atmosphere-ocean redox conditions that are linked to biological evolution, for example, the activity of oxygen-producing, photosynthetic cyanobacteria. In this review, we summarize available Precambrian trace element proxy data, and discuss how temporal trends in the seawater concentrations of specific trace elements may be linked to the evolution of both simple and complex life. We also examine several biologically relevant and/or redox-sensitive trace elements that have yet to be fully examined in the sedimentary rock record (e.g., Cu, Cd, W) and suggest several directions for future studies.
Stealing prey plastids for metabolic gain is a common phenomenon among protists within aquatic ecosystems.1 Ciliates of the Mesodinium rubrum species complex are unique in that they also steal a ...transcriptionally active but non-dividing prey nucleus, the kleptokaryon, from certain cryptophytes.2 The kleptokaryon enables full control and replication of kleptoplastids but has a half-life of about 10 days.2 Once the kleptokaryon is lost, the ciliate experiences a slow loss of photosynthetic metabolism and eventually death.2,3,4 This transient ability to function phototrophically allows M. rubrum to form productive blooms in coastal waters.5,6,7,8 Here, we show, using multi-omics approaches, that an Antarctic strain of the ciliate not only depends on stolen Geminigera cryophila organelles for photosynthesis but also for anabolic synthesis of fatty acids, amino acids, and other essential macromolecules. Transcription of diverse pathways was higher in the kleptokaryon than that in G. cryophila, and many increased in higher light. Proteins of major biosynthetic pathways were found in greater numbers in the kleptokaryon relative to M. rubrum, implying anabolic dependency on foreign metabolism. We show that despite losing transcriptional control of the kleptokaryon, M. rubrum regulates kleptoplastid pigments with changing light, implying an important role for post-transcriptional control. These findings demonstrate that the integration of foreign organelles and their gene and protein expression, energy metabolism, and anabolism occur in the absence of a stable endosymbiotic association. Our results shed light on potential events early in the process of complex plastid acquisition and broaden our understanding of symbiogenesis.
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•M. rubrum steals prey nucleus (kleptokaryon) to acquire its metabolism•M. rubrum remodels biosynthetic pathways of prey•Kleptokaryon genes in M. rubrum lack fine-tuned regulation•Ability to photoacclimate implies post-transcriptional regulation
Johnson et al. show that the enslaved algal nucleus in Mesodinium rubrum is highly active transcriptionally but lacks fine-tuned regulation. Despite this, it retains the ability to regulate kleptoplastid pigment levels. Proteome and metabolome data reveal that the ciliate depends upon its stolen organelles for most of its biosynthetic needs.
In many oceanic regions, anthropogenic warming will coincide with iron (Fe) limitation. Interactive effects between warming and Fe limitation on phytoplankton physiology and biochemical function are ...likely, as temperature and Fe availability affect many of the same essential cellular pathways. However, we lack a clear understanding of how globally significant phytoplankton such as the picocyanobacteria
will respond to these co-occurring stressors, and what underlying molecular mechanisms will drive this response. Moreover, ecotype-specific adaptations can lead to nuanced differences in responses between strains. In this study,
isolates YX04-1 (oceanic) and XM-24 (coastal) from the South China Sea were acclimated to Fe limitation at two temperatures, and their physiological and proteomic responses were compared. Both strains exhibited reduced growth due to warming and Fe limitation. However, coastal XM-24 maintained relatively higher growth rates in response to warming under replete Fe, while its growth was notably more compromised under Fe limitation at both temperatures compared with YX04-1. In response to concurrent heat and Fe stress, oceanic YX04-1 was better able to adjust its photosynthetic proteins and minimize the generation of reactive oxygen species while reducing proteome Fe demand. Its intricate proteomic response likely enabled oceanic YX04-1 to mitigate some of the negative impact of warming on its growth during Fe limitation. Our study highlights how ecologically-shaped adaptations in
strains even from proximate oceanic regions can lead to differing physiological and proteomic responses to these climate stressors.
Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can ...be co-limited by cobalamin (vitamin B
). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophyte
. However, the vitamin requirements and ecophysiology of the keystone species
remain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response of
to a matrix of Fe-B
conditions. We show that
is not auxotrophic for B
, as previously suggested, and identify mechanisms underlying its B
response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B
-independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B
-dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiple
species and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding that
has a flexible B
metabolism has implications for its relative fitness compared to B
-auxotrophic diatoms and for the detection of B
-stress in a more diverse set of marine microbes.
Persistence of deeply sourced iron in the Pacific Ocean Horner, Tristan J.; Williams, Helen M.; Hein, James R. ...
Proceedings of the National Academy of Sciences - PNAS,
02/2015, Letnik:
112, Številka:
5
Journal Article
Recenzirano
Odprti dostop
Biological carbon fixation is limited by the supply of Fe in vast regions of the global ocean. Dissolved Fe in seawater is primarily sourced from continental mineral dust, submarine hydrothermalism, ...and sediment dissolution along continental margins. However, the relative contributions of these three sources to the Fe budget of the open ocean remains contentious. By exploiting the Fe stable isotopic fingerprints of these sources, it is possible to trace distinct Fe pools through marine environments, and through time using sedimentary records. We present a reconstruction of deep-sea Fe isotopic compositions from a Pacific Fe−Mn crust spanning the past 76 My. We find that there have been large and systematic changes in the Fe isotopic composition of seawater over the Cenozoic that reflect the influence of several, distinct Fe sources to the central Pacific Ocean. Given that deeply sourced Fe from hydrothermalism and marginal sediment dissolution exhibit the largest Fe isotopic variations in modern oceanic settings, the record requires that these deep Fe sources have exerted a major control over the Fe inventory of the Pacific for the past 76 My. The persistence of deeply sourced Fe in the Pacific Ocean illustrates that multiple sources contribute to the total Fe budget of the ocean and highlights the importance of oceanic circulation in determining if deeply sourced Fe is ever ventilated at the surface.
Significance The vertical supply of dissolved Fe (iron) is insufficient compared with the physiological needs of marine phytoplankton in vast swathes of the open ocean. However, the relative importance of the main sources of “new” Fe to the ocean—continental mineral dust, hydrothermal exhalations, and sediment dissolution—and their temporal evolution are poorly constrained. By analyzing the isotopic composition of Fe in marine sediments, we find that much of the dissolved Fe in the central Pacific Ocean originated from hydrothermal and sedimentary sources thousands of meters below the sea surface. As such, these data underscore the vital role of the oceans’ physical mixing in determining if any deeply sourced Fe ever reaches the Fe-starved surface-dwelling biota.
Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can ...be co-limited by cobalamin (vitamin B12). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophyte Phaeocystis antarctica. However, the vitamin requirements and ecophysiology of the keystone species P. antarctica remain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response of P. antarctica to a matrix of Fe-B12 conditions. We show that P. antarctica is not auxotrophic for B12, as previously suggested, and identify mechanisms underlying its B12 response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B12-independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B12-dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiple Phaeocystis species and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding that P. antarctica has a flexible B12 metabolism has implications for its relative fitness compared to B12-auxotrophic diatoms and for the detection of B12-stress in a more diverse set of marine microbes.
Cobalt is an important micronutrient for ocean microbes as it is present in vitamin B12 and is a co‐factor in various metalloenzymes that catalyze cellular processes. Moreover, when seawater ...availability of cobalt is compared to biological demands, cobalt emerges as being depleted in seawater, pointing to a potentially important limiting role. To properly account for the potential biological role for cobalt, there is therefore a need to understand the processes driving the biogeochemical cycling of cobalt and, in particular, the balance between external inputs and internal cycling. To do so, we developed the first cobalt model within a state‐of‐the‐art three‐dimensional global ocean biogeochemical model. Overall, our model does a good job in reproducing measurements with a correlation coefficient of >0.7 in the surface and >0.5 at depth. We find that continental margins are the dominant source of cobalt, with a crucial role played by supply under low bottom‐water oxygen conditions. The basin‐scale distribution of cobalt supplied from margins is facilitated by the activity of manganese‐oxidizing bacteria being suppressed under low oxygen and low temperatures, which extends the residence time of cobalt. Overall, we find a residence time of 7 and 250 years in the upper 250 m and global ocean, respectively. Importantly, we find that the dominant internal resupply process switches from regeneration and recycling of particulate cobalt to dissolution of scavenged cobalt between the upper ocean and the ocean interior. Our model highlights key regions of the ocean where biological activity may be most sensitive to cobalt availability.
Plain Language Summary
Biological activity in the sea requires cobalt, primarily due to its role in vitamin B12 but also because it is required in other cellular enzymes. While our observations of cobalt distributions in the ocean is growing, we do not have a quantitative understanding of the role of different external sources of cobalt or how it is internally processed by different biological and chemical processes in the ocean. To answer these questions, we built the first ever global ocean cobalt model that coupled the cycling of cobalt to the major biogeochemical processes occurring in the ocean. Using this model, we identified that sediments are the major cobalt source and that the combination of oxygen levels and scavenging removal by bacteria allow externally supplied cobalt to pervade the ocean as a whole. We find that in certain regions of the upper ocean, cobalt levels may be low enough to affect biological activity but that to quantify this requires further work on how we represent cellular biochemistry.
Key Points
The first global model of ocean cobalt cycling is presented
Sediments are the major global source of cobalt
Suppression of Co scavenging by low oxygen and reduced bacterial activity is key in extending the residence time of externally supplied Co
Cobalt (Co) is an important bioactive trace metal that is the metal
cofactor in cobalamin (vitamin B12) which can limit or co-limit
phytoplankton growth in many regions of the ocean. Total dissolved ...and
labile Co measurements in the Canadian sector of the Arctic Ocean during the
U.S. GEOTRACES Arctic expedition (GN01) and the Canadian International Polar
Year GEOTRACES expedition (GIPY14) revealed a dynamic biogeochemical cycle
for Co in this basin. The major sources of Co in the Arctic were from shelf
regions and rivers, with only minimal contributions from other freshwater
sources (sea ice, snow) and eolian deposition. The most striking feature
was the extremely high concentrations of dissolved Co in the upper 100 m,
with concentrations routinely exceeding 800 pmol L−1 over the shelf
regions. This plume of high Co persisted throughout the Arctic basin and
extended to the North Pole, where sources of Co shifted from primarily
shelf-derived to riverine, as freshwater from Arctic rivers was entrained in
the Transpolar Drift. Dissolved Co was also strongly organically complexed
in the Arctic, ranging from 70 % to 100 % complexed in the surface and deep
ocean, respectively. Deep-water concentrations of dissolved Co were
remarkably consistent throughout the basin (∼55 pmol L−1), with concentrations reflecting those of deep Atlantic water and
deep-ocean scavenging of dissolved Co. A biogeochemical model of Co cycling
was used to support the hypothesis that the majority of the high surface Co
in the Arctic was emanating from the shelf. The model showed that the high
concentrations of Co observed were due to the large shelf area of the
Arctic, as well as to dampened scavenging of Co by manganese-oxidizing (Mn-oxidizing)
bacteria due to the lower temperatures. The majority of this scavenging
appears to have occurred in the upper 200 m, with minimal additional
scavenging below this depth. Evidence suggests that both dissolved Co (dCo) and labile Co (LCo) are increasing over time on the Arctic shelf, and these limited temporal results are consistent
with other tracers in the Arctic. These
elevated surface concentrations of Co likely lead to a net flux of Co out of
the Arctic, with implications for downstream biological uptake of Co in the
North Atlantic and elevated Co in North Atlantic Deep Water. Understanding
the current distributions of Co in the Arctic will be important for
constraining changes to Co inputs resulting from regional intensification of
freshwater fluxes from ice and permafrost melt in response to ongoing
climate change.
One-quarter of photosynthesis-derived carbon on Earth rapidly cycles through a set of short-lived seawater metabolites that are generated from the activities of marine phytoplankton, bacteria, ...grazers and viruses. Here we discuss the sources of microbial metabolites in the surface ocean, their roles in ecology and biogeochemistry, and approaches that can be used to analyse them from chemistry, biology, modelling and data science. Although microbial-derived metabolites account for only a minor fraction of the total reservoir of marine dissolved organic carbon, their flux and fate underpins the central role of the ocean in sustaining life on Earth.
In this study, we develop a mechanistic understanding of how temperature affects growth and photosynthesis in 10 geographically and physiologically diverse strains of Synechococcus spp. We found that ...Synechococcus spp. are able to regulate photochemistry over a range of temperatures by using state transitions and altering the abundance of photosynthetic proteins. These strategies minimize photosystem II (PSII) photodamage by keeping the photosynthetic electron transport chain (ETC), and hence PSII reaction centers, more oxidized. At temperatures that approach the optimal growth temperature of each strain when cellular demand for reduced nicotinamide adenine dinucleotide phosphate (NADPH) is greatest, the phycobilisome (PBS) antenna associates with PSII, increasing the flux of electrons into the ETC. By contrast, under low temperature, when slow growth lowers the demand for NADPH and linear ETC declines, the PBS associates with photosystem I. This favors oxidation of PSII and potential increase in cyclic electron flow. For Synechococcus sp. WH8102, growth at higher temperatures led to an increase in the abundance of PBS pigment proteins, as well as higher abundance of subunits of the PSII, photosystem I, and cytochrome b6f complexes. This would allow cells to increase photosynthetic electron flux to meet the metabolic requirement for NADPH during rapid growth. These PBS-based temperature acclimation strategies may underlie the larger geographic range of this group relative to Prochlorococcus spp., which lack a PBS.
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