Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae

Reusing growth medium (water supplemented with nutrients) for microalgae cultivation is required for economical and environmentally sustainable production of algae bioproducts (fuels, feed, and food). However, reused medium often contains microbes and dissolved organic matter that may affect algae growth. While the accumulation of dissolved organic carbon (DOC) in reused medium has been demonstrated, it is unclear whether DOC concentrations affect algae growth or subsequent rates of algal DOC release. To address these questions, lab-scale experiments were conducted with three marine microalgae strains, Navicula sp. SFP, Staurosira sp. C323, and Chlorella sp. D046, grown in medium reused up to four times. Navicula sp. and Chlorella sp. grew similarly in reused medium as in fresh medium, while Staurosira sp. became completely inhibited in reused medium. Across the three algae, there was no broad trend between initial DOC concentration in reused medium and algae growth response. Navicula sp. released less DOC overall in reused medium than in fresh medium, but DOC release rates did not decrease proportionally with increased DOC concentrations. Net DOC accumulation was much lower than gross DOC released by Navicula sp. and Staurosira sp., indicating the majority of released DOC was degraded. Additionally, biodegradation experiments with reused media showed no further net decrease in DOC, suggesting the accumulated DOC was recalcitrant to the associated bacteria. Overall, these results suggest that taxa-specific factors may be responsible for algae growth response in reused medium, and that DOC release and accumulation are insensitive to prior cultivation rounds. Choosing an algae strain that is uninhibited by accumulated DOC is therefore critical to ensure successful water reuse in the algae industry

Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface

The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species

Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean\u27s Surface

The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species. DOI: 10.1371/journal.pone.001680

Global Gene Expression of Prochlorococcus ecotypes in Response to Changes in Nitrogen Availability

Nitrogen (N) often limits biological productivity in the oceanic gyres where Prochlorococcus is the most abundant photosynthetic organism. The Prochlorococcus community is composed of strains, such as MED4 and MIT9313, that have different N utilization capabilities and that belong to ecotypes with different depth distributions. An interstrain comparison of how Prochlorococcus responds to changes in ambient nitrogen is thus central to understanding its ecology. We quantified changes in MED4 and MIT9313 global mRNA expression, chlorophyll fluorescence, and photosystem II photochemical efficiency (Fv/Fm) along a time series of increasing N starvation. In addition, the global expression of both strains growing in ammonium-replete medium was compared to expression during growth on alternative N sources. There were interstrain similarities in N regulation such as the activation of a putative NtcA regulon during N stress. There were also important differences between the strains such as in the expression patterns of carbon metabolism genes, suggesting that the two strains integrate N and C metabolism in fundamentally different ways

The effect of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean

The deep chlorophyll maximum (DCM) is a widespread feature in most stratified, oligotrophic waters. In addition to their well-established importance for many surface phytoplankton communities, more recent evidence suggests that iron, light or co-limitation may also be important drivers for some DCM communities. To test this hypothesis, we describe the results from six grow-out experiments, four from the Equatorial Pacific Ocean (between 150°E and 140°W), one in Western Pacific Warm Pool (9°S, 170°E) and one in the middle of the Tasman Sea (36°S). Photosynthetic efficiency (Fv/Fm) and biomass response, including Chl a and phytoplankton community structure (pennate diatoms, photosynthetic eukaryotes, Synechococcus, Prochlorococcus, and major Prochlorococcus ecotypes), were assessed over five days in control, +Fe, +Light or +Fe +Light treatments. Photosynthetic efficiency did not change dramatically in any of the treatments at any of the locations, except at 0°N 140°W where the control and +Fe bottles had elevated efficiency relative to both +Light treatments. Except for some ecotypes of Prochlorococcus (eMIT9313 and eNATL2A), phytoplankton populations were most strongly limited by light in the DCM. Pennate diatoms and other photosynthetic eukaryotes showed the most enhancement with the addition of iron and light at some stations and may be co-limited, but no phytoplankton populations were enhanced by adding iron alone. Although the duration and magnitude of the responses varied depending on initial macronutrient concentrations, they were generally consistent across the locations sampled. These results suggest that light is the primary limiting resource of the DCM for this vast region, but that iron can play an important additive role in limiting phytoplankton populations in locations where flux to the DCM is reduced

Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability

Nitrogen (N) often limits biological productivity in the oceanic gyres where Prochlorococcus is the most abundant photosynthetic organism. The Prochlorococcus community is composed of strains, such as MED4 and MIT9313, that have different N utilization capabilities and that belong to ecotypes with different depth distributions. An interstrain comparison of how Prochlorococcus responds to changes in ambient nitrogen is thus central to understanding its ecology. We quantified changes in MED4 and MIT9313 global mRNA expression, chlorophyll fluorescence, and photosystem II photochemical efficiency (F(v)/F(m)) along a time series of increasing N starvation. In addition, the global expression of both strains growing in ammonium-replete medium was compared to expression during growth on alternative N sources. There were interstrain similarities in N regulation such as the activation of a putative NtcA regulon during N stress. There were also important differences between the strains such as in the expression patterns of carbon metabolism genes, suggesting that the two strains integrate N and C metabolism in fundamentally different ways

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean. © 2015, National Academy of Sciences. All rights reserved

The challenges of detecting and attributing ocean acidification impacts on marine ecosystems

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Doo, S. S., Kealoha, A., Andersson, A., Cohen, A. L., Hicks, T. L., Johnson, Z., I., Long, M. H., McElhany, P., Mollica, N., Shamberger, K. E. F., Silbiger, N. J., Takeshita, Y., & Busch, D. S. The challenges of detecting and attributing ocean acidification impacts on marine ecosystems. ICES Journal of Marine Science, 77(7-8), (2020): 2411-2422, https://doi.org/10.1093/icesjms/fsaa094.A substantial body of research now exists demonstrating sensitivities of marine organisms to ocean acidification (OA) in laboratory settings. However, corresponding in situ observations of marine species or ecosystem changes that can be unequivocally attributed to anthropogenic OA are limited. Challenges remain in detecting and attributing OA effects in nature, in part because multiple environmental changes are co-occurring with OA, all of which have the potential to influence marine ecosystem responses. Furthermore, the change in ocean pH since the industrial revolution is small relative to the natural variability within many systems, making it difficult to detect, and in some cases, has yet to cross physiological thresholds. The small number of studies that clearly document OA impacts in nature cannot be interpreted as a lack of larger-scale attributable impacts at the present time or in the future but highlights the need for innovative research approaches and analyses. We summarize the general findings in four relatively well-studied marine groups (seagrasses, pteropods, oysters, and coral reefs) and integrate overarching themes to highlight the challenges involved in detecting and attributing the effects of OA in natural environments. We then discuss four potential strategies to better evaluate and attribute OA impacts on species and ecosystems. First, we highlight the need for work quantifying the anthropogenic input of CO2 in coastal and open-ocean waters to understand how this increase in CO2 interacts with other physical and chemical factors to drive organismal conditions. Second, understanding OA-induced changes in population-level demography, potentially increased sensitivities in certain life stages, and how these effects scale to ecosystem-level processes (e.g. community metabolism) will improve our ability to attribute impacts to OA among co-varying parameters. Third, there is a great need to understand the potential modulation of OA impacts through the interplay of ecology and evolution (eco–evo dynamics). Lastly, further research efforts designed to detect, quantify, and project the effects of OA on marine organisms and ecosystems utilizing a comparative approach with long-term data sets will also provide critical information for informing the management of marine ecosystems.SSD was funded by NSF OCE (grant # 1415268). DSB and PM were supported by the NOAA Ocean Acidification Program and Northwest Fisheries Science Center, MHL was supported by NSF OCE (grant # 1633951), ZIJ was supported by NSF OCE (grant # 1416665) and DOE EERE (grant #DE-EE008518), NJS was supported by NSF OCE (grant # 1924281), ALC was supported by NSF OCE (grant # 1737311), and AA was supported by NSF OCE (grant # 1416518). KEFS, AK, and TLH were supported by Texas A&M University. This is CSUN Marine Biology contribution (# 306)

State of the Carbon Cycle - Consequences of Rising Atmospheric CO2

The rise of atmospheric CO2, largely attributable to human activity through fossil fuel emissions and land-use change, has been dampened by carbon uptake by the ocean and terrestrial biosphere. We outline the consequences of this carbon uptake as direct and indirect effects on terrestrial and oceanic systems and processes for different regions of North America and the globe. We assess the capacity of these systems to continue to act as carbon sinks. Rising CO2 has decreased seawater pH; this process of ocean acidification has impacted some marine species and altered fundamental ecosystem processes with further effects likely. In terrestrial ecosystems, increased atmospheric CO2 causes enhanced photosynthesis, net primary production, and increased water-use efficiency. Rising CO2 may change vegetation composition and carbon storage, and widespread increases in water use efficiency likely influence terrestrial hydrology and biogeochemical cycling. Consequences for human populations include changes to ecosystem services including cultural activities surrounding land use, agricultural or harvesting practices. Commercial fish stocks have been impacted and crop production yields have been changed as a result of rising CO2. Ocean and terrestrial effects are contingent on, and feedback to, global climate change. Warming and modified precipitation regimes impact a variety of ecosystem processes, and the combination of climate change and rising CO2 contributes considerable uncertainty to forecasting carbon sink capacity in the ocean and on land. Disturbance regime (fire and insects) are modified with increased temperatures. Fire frequency and intensity increase, and insect lifecycles are disrupted as temperatures move out of historical norms. Changes in disturbance patterns modulate the effects of rising CO2 depending on ecosystem type, disturbance frequency, and magnitude of events. We discuss management strategies designed to limit the rise of atmospheric CO2 and reduce uncertainty in forecasts of decadal and centennial feedbacks of rising atmospheric CO2 on carbon storage

Phosphate (PO4) and Silicate (SiOH4) concentrations from R/V Thomas G. Thompson and R/V Kilo Moana cruises TN277, KM1301, KM1312 in the Eastern North Pacific Ocean from 2012-2013 (POWOW project)

Dataset: PO4_SiOH4Phosphate (PO4) and Silicate (SiOH4) concentrations from R/V Thomas G. Thompson and R/V Kilo Moana cruises TN277, KM1301, KM1312 in the Eastern North Pacific Ocean from 2012-2013 (POWOW project) For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/3756NSF Division of Ocean Sciences (NSF OCE) OCE-103106