RESUMEN
Coccolithophores play a significant role in marine calcium carbonate production and carbon cycles, attributing to their unique feature of producing calcareous plates, coccoliths. Coccolithophores also possess a haplo-diplontic life cycle, presenting distinct morphology types and calcification states. However, differences in nutrient acquisition strategies and mixotrophic behaviors of the two life phases remain unclear. In this study, we conducted a series of phagocytosis experiments of calcified diploid and non-calcified haploid strains of coccolithophore Gephyrocapsa huxleyi under light and dark conditions. The phagocytosis capability of each strain was examined based on characteristic fluorescent signals from ingested beads using flow cytometry and fluorescence microscopy. The results show a significantly higher phagocytosis percentage on fluorescent beads in the bacterial prey surrogates of the non-calcified haploid Gephyrocapsa huxleyi strain, than the calcified diploid strain with or without light. In addition, the non-calcified diploid cells seemingly to presented a much higher phagocytosis percentage in darkness than under light. The differential phagocytosis capacities between the calcified diploid and non-calcified haploid Gephyrocapsa huxleyi strains indicate potential distinct nutritional strategies at different coccolithophore life and calcifying stages, which may further shed light on the potential strategies that coccolithophore possesses in unfavorable environments such as twilight zones and the expanding coccolithophore niches in the natural marine environment under the climate change scenario.
RESUMEN
Ocean microbes are involved in global processes such as nutrient and carbon cycling. Recent studies indicated diverse modes of algal-bacterial interactions, including mutualism and pathogenicity, which have a substantial impact on ecology and oceanic carbon sequestration, and hence, on climate. However, the airborne dispersal and pathogenicity of bacteria in the marine ecosystem remained elusive. Here, we isolated an airborne algicidal bacterium, Roseovarius nubinhibens, emitted to the atmosphere as primary marine aerosol (referred also as sea spray aerosols) and collected above a coccolithophore bloom in the North Atlantic Ocean. The aerosolized bacteria retained infective properties and induced lysis of Gephyrocapsa huxleyi cultures.This suggests that the transport of marine bacteria through the atmosphere can effectively spread infection agents over vast oceanic regions, highlighting its significance in regulating the cell fate in algal blooms.
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Fitoplancton , Agua de Mar , Fitoplancton/fisiología , Agua de Mar/microbiología , Ecosistema , Océanos y Mares , Bacterias/genéticaRESUMEN
To investigate effects of UV radiation (UVR, 280-400â¯nm) on coccolithophorids under nutrient-limited conditions, we grew Gephyrocapsa oceanica to determine its resilience to consecutive daily short-term exposures to +UVR (irradiances >295â¯nm) under a range of nitrate availabilities (100, 24, 12, 6 and 3⯵M). +UVR alone significantly hampered the growth of G. oceanica, with the synergistic negative effects of +UVR and N-limitation being about 58% and 22% greater than under UVR or N-limitation alone, respectively. Most 3⯵M nitrate cultures died, but those exposed to UVR succumbed sooner. This was due to a failure of photoprotection and repair mechanisms under low N-availability with exposures to UVR. Additionally, the UVR-induced inhibition of the effective quantum yield of photosystem II (PSII) was significantly higher and was further aggravated by N limitation. The algal cells increased photoprotective pigments and UV-absorbing compounds as a priority rather than using calcification for defense against UVR, indicating a trade-off in energy and resource allocation. Our results indicate the negative effects of UVR on coccolithophorid growth and photosynthesis, and highlight the important role of N availability in defense against UVR as well as high PAR. We predict that enhanced N-limitation in future surface oceans due to warming-induced stratification will exacerbate the sensitivity of G. oceanica to UVR, while coccolithophores can be potentially more susceptible to other environmental stresses due to increased levels of nutrient limitation.
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HaptophytaRESUMEN
Rising ocean temperatures will alter the diversity of marine phytoplankton communities, likely leading to modifications in food-web and biogeochemical dynamics. Here we focus on coccolithophores, a prominent group of calcifying phytoplankton that plays a central role in the global carbon cycle. Using both new (2017-2020) and historical (1975-1976) data from the northern Red Sea, we found that during 'mild summers', the most common coccolithophores - Emiliania huxleyi and Gephyrocapsa ericsonii - co-exist at similar densities. Both species then particularly flourish during subsequent winter periods where nutrient availability is higher due to convective mixing. However, during 'hot summers', which have become progressively the norm over the last decades with average surface temperatures exceeding 27°C for long time-periods, G. ericsonii density markedly declined. Moreover, G. ericsonii remains at low background levels even during winter mixing periods, while E. huxleyi succession and development during winter appears unchanged. Further incubation assays using native assemblages confirmed that G. ericsonii's growth over 27°C is significantly reduced relative to E. huxleyi. Additional factors likely contribute to impair G. ericsonii populations at sea, but temperature is a key factor. Our results illustrate the divergent impact of ongoing ocean warming in tropical phytoplankton species.
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Ecosistema , Haptophyta , Fitoplancton , Estaciones del Año , TemperaturaRESUMEN
Coccolithophores are important oceanic primary producers not only in terms of photosynthesis but also because they produce calcite plates called coccoliths. Ongoing ocean acidification associated with changing seawater carbonate chemistry may impair calcification and other metabolic functions in coccolithophores. While short-term ocean acidification effects on calcification and other properties have been examined in a variety of coccolithophore species, long-term adaptive responses have scarcely been documented, other than for the single species Emiliania huxleyi. Here, we investigated the effects of ocean acidification on another ecologically important coccolithophore species, Gephyrocapsa oceanica, following 1,000 generations of growth under elevated CO2 conditions (1,000 µatm). High CO2 -selected populations exhibited reduced growth rates and enhanced particulate organic carbon (POC) and nitrogen (PON) production, relative to populations selected under ambient CO2 (400 µatm). Particulate inorganic carbon (PIC) and PIC/POC ratios decreased progressively throughout the selection period in high CO2 -selected cell lines. All of these trait changes persisted when high CO2 -grown populations were moved back to ambient CO2 conditions for about 10 generations. The results suggest that the calcification of some coccolithophores may be more heavily impaired by ocean acidification than previously predicted based on short-term studies, with potentially large implications for the ocean's carbon cycle under accelerating anthropogenic influences.
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Adaptación Fisiológica/genética , Dióxido de Carbono/administración & dosificación , Dióxido de Carbono/farmacología , Haptophyta/efectos de los fármacos , Selección Genética , Carbono/metabolismo , Carbonatos/metabolismo , Haptophyta/genética , Haptophyta/crecimiento & desarrollo , Concentración de Iones de Hidrógeno , Nitrógeno/metabolismo , Fotosíntesis/efectos de los fármacos , Agua de Mar/químicaRESUMEN
Phenotypic plasticity describes the phenotypic adjustment of the same genotype to different environmental conditions and is best described by a reaction norm. We focus on the effect of ocean acidification on inter- and intraspecific reaction norms of three globally important phytoplankton species (Emiliania huxleyi, Gephyrocapsa oceanica and Chaetoceros affinis). Despite significant differences in growth rates between the species, they all showed a high potential for phenotypic buffering (similar growth rates between ambient and high CO2 conditions). Only three coccolithophore genotypes showed a reduced growth in high CO2 Diverging responses to high CO2 of single coccolithophore genotypes compared with the respective mean species responses, however, raise the question of whether an extrapolation to the population level is possible from single-genotype experiments. We therefore compared the mean response of all tested genotypes with a total species response comprising the same genotypes, which was not significantly different in the coccolithophores. Assessing species reaction norms to different environmental conditions on short time scale in a genotype-mix could thus reduce sampling effort while increasing predictive power.
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Dióxido de Carbono/fisiología , Diatomeas/crecimiento & desarrollo , Haptophyta/crecimiento & desarrollo , Agua de Mar/química , Dióxido de Carbono/toxicidad , Diatomeas/genética , Haptophyta/genética , Concentración de Iones de Hidrógeno , Océanos y Mares , Fenotipo , Fitoplancton/genética , Fitoplancton/crecimiento & desarrollo , Especificidad de la EspecieRESUMEN
The coccolithophore family Noëlaerhabdaceae contains a number of taxa that are very abundant in modern oceans, including the cosmopolitan bloom-forming Emiliania huxleyi. Introgressive hybridization has been suggested to account for incongruences between nuclear, mitochondrial and plastidial phylogenies of morphospecies within this lineage, but the number of species cultured to date remains rather limited. Here, we present the characterization of 5 new Noëlaerhabdaceae culture strains isolated from samples collected in the south-east Pacific Ocean. These were analyzed morphologically using scanning electron microscopy and phylogenetically by sequencing 5 marker genes (nuclear 18S and 28S rDNA, plastidial tufA, and mitochondrial cox1 and cox3 genes). Morphologically, one of these strains corresponded to Gephyrocapsa ericsonii and the four others to Reticulofenestra parvula. Ribosomal gene sequences were near identical between these new strains, but divergent from G. oceanica, G. muellerae, and E. huxleyi. In contrast to the clear distinction in ribosomal phylogenies, sequences from other genomic compartments clustered with those of E. huxleyi strains with which they share an ecological range (i.e., warm temperate to tropical waters). These data provide strong support for the hypothesis of past (and potentially ongoing) introgressive hybridization within this ecologically important lineage and for the transfer of R. parvula to Gephyrocapsa. These results have important implications for understanding the role of hybridization in speciation in vast ocean meta-populations of phytoplankton.
RESUMEN
The coccolithophore genus Gephyrocapsa contains a cosmopolitan assemblage of pelagic species, including the bloom-forming Gephyrocapsa oceanica, and is closely related to the emblematic coccolithophore Emiliania huxleyi within the Noëlaerhabdaceae. These two species have been extensively studied and are well represented in culture collections, whereas cultures of other species of this family are lacking. We report on three new strains of Gephyrocapsa isolated into culture from samples from the Chilean coastal upwelling zone using a novel flow cytometric single-cell sorting technique. The strains were characterized by morphological analysis using scanning electron microscopy and phylogenetic analysis of 6 genes (nuclear 18S and 28S rDNA, plastidial 16S and tufA, and mitochondrial cox1 and cox3 genes). Morphometric features of the coccoliths indicate that these isolates are distinct from G. oceanica and best correspond to G. muellerae. Surprisingly, both plastidial and mitochondrial gene phylogenies placed these strains within the E. huxleyi clade and well separated from G. oceanica isolates, making Emiliania appear polyphyletic. The only nuclear sequence difference, 1bp in the 28S rDNA region, also grouped E. huxleyi with the new Gephyrocapsa isolates and apart from G. oceanica. Specifically, the G. muellerae morphotype strains clustered with the mitochondrial ß clade of E. huxleyi, which, like G. muellerae, has been associated with cold (temperate and sub-polar) waters. Among putative evolutionary scenarios that could explain these results we discuss the possibility that E. huxleyi is not a valid taxonomic unit, or, alternatively the possibility of past hybridization and introgression between each E. huxleyi clade and older Gephyrocapsa clades. In either case, the results support the transfer of Emiliania to Gephyrocapsa. These results have important implications for relating morphological species concepts to ecological and evolutionary units of diversity.
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Haptophyta/clasificación , Haptophyta/ultraestructura , Filogenia , Biodiversidad , Chile , Genes Protozoarios/genética , Haptophyta/genética , Haptophyta/aislamiento & purificación , Océano Pacífico , Especificidad de la EspecieRESUMEN
The hydrocarbons in cultures of marine haptophytes Emiliania huxleyi NIES837 and Gephyrocapsa oceanica NIES1315 were analyzed, and nonacosadienes and hentriacontadienes were detected as the major compounds in both strains. C29 and C31 monoenes and di-, tri- and tetra-unsaturated C33 alkenes were also detected as minor compounds but not C37 and C38 alkenes. The positions of the double bonds in the C29 and C31 alkenes were determined by mass spectrometry of their dimethyl disulfide (DMDS) adducts. Among the four C29 alkenes identified, the most abundant isomer was 2,20-nonacosadiene, and the other three compounds were 1,20-nonacosadiene, 3,20-nonacosadiene and 9-nonacosene, respectively. Hitherto, 2,20-nonacosadiene and 3,20-nonacosadiene were unknown to be natural products. The double bond at the n-9 (ω9) position in these C29 alkenes is hypothesized to be derived from precursors of unsaturated fatty acids possessing an n-9 double bond, such as (9Z)-9-octadecenoic acid. Nonacosadienes have the potential for being used as distinct haptophyte biomarkers.
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Alcadienos/aislamiento & purificación , Haptophyta/química , Alcadienos/química , Cromatografía de Gases y Espectrometría de Masas , Biología Marina , Estructura Molecular , Ácido Oléico/química , Ácidos Oléicos , EstereoisomerismoRESUMEN
Emiliania huxleyi and Gephyrocapsa oceanica are abundant coccolithophore morpho-species that play key roles in ocean carbon cycling due to their importance as both primary producers and cal-cifiers. Global change processes such as ocean acidification impact these key calcifying species. The physiology of E. huxleyi, a developing model species, has been widely studied, but its genetic delineation from G. oceanica remains unclear due to a lack of resolution in classical genetic markers. Using nuclear (18S rDNA and 28S rDNA), mitochondrial (cox1, cox2, cox3, rpl16, and dam), and plastidial (16S rDNA, rbcL, tufA, and petA) DNA markers from 99 E. huxleyi and 44 G. oceanica strains, we conducted a multigene/multistrain survey to compare the suitability of different markers for resolving phylogenetic patterns within and between these two morpho-species. The nuclear genes tested did not provide sufficient resolution to discriminate between the two morpho-species that diverged only 291Kya. Typical patterns of incomplete lineage sorting were generated in phylogenetic analyses using plastidial genes. In contrast, full morpho-species delineation was achieved with mitochondrial markers and common intra-morpho-species phylogenetic patterns were observed despite differing rates of DNA substitution. Mitochondrial genes are thus promising barcodes for distinguishing these coccolithophore morpho-species, in particular in the context of environmental monitoring.
RESUMEN
The ongoing ocean acidification associated with a changing carbonate system may impose profound effects on marine planktonic calcifiers. Here, we show that a coccolithophore, Gephyrocapsa oceanica, evolved in response to an elevated CO2 concentration of 1000 µatm (pH reduced to 7.8) in a long-term (â¼670 generations) selection experiment. The high CO2 -selected cells showed increases in photosynthetic carbon fixation, growth rate, cellular particulate organic carbon (POC) or nitrogen (PON) production, and a decrease in C:N elemental ratio, indicating a greater upregulation of PON than of POC production under the ocean acidification condition. Cells from the low CO2 selection process shifted to high CO2 exposure showed an enhanced cellular POC and PON production rates. Our data suggest that the coccolithophorid could adapt to ocean acidification with enhanced assimilations of carbon and nitrogen but decreased C:N ratios.