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Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean.

ABSTRACT: Assessing the iron (Fe) nutritional status of natural diatom populations has proven challenging as physiological and molecular responses can differ in diatoms of the same genus. We evaluated expression of genes encoding flavodoxin (FLDA1) and an Fe-starvation induced protein (ISIP3) as indicators of Fe limitation in the marine diatom Thalassiosira oceanica. The specificity of the response to Fe limitation was tested in cultures grown under Fe- and macronutrient-deficient conditions, as well as throughout the diurnal light cycle. Both genes showed a robust and specific response to Fe limitation in laboratory cultures and were detected in small volume samples collected from the northeast Pacific, demonstrating the sensitivity of this method. Overall, FLDA1 and ISIP3 expression was inversely related to Fe concentrations and offered insight into the Fe nutritional health of T. oceanica in the field. As T. oceanica is a species tolerant to low Fe, indications of Fe limitation in T. oceanica populations may serve as a proxy for severe Fe stress in the overall diatom community. At two shallow coastal locations, FLD1A and ISIP3 expression revealed Fe stress in areas where dissolved Fe concentrations were high, demonstrating that this approach may be powerful for identifying regions where Fe supply may not be biologically available.

SUBMITTER: Chappell PD

PROVIDER: S-EPMC4331588 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean.

Chappell P Dreux PD Whitney LeAnn P LP Wallace Joselynn R JR Darer Adam I AI Jean-Charles Samua S Jenkins Bethany D BD

The ISME journal 20141021 3

Assessing the iron (Fe) nutritional status of natural diatom populations has proven challenging as physiological and molecular responses can differ in diatoms of the same genus. We evaluated expression of genes encoding flavodoxin (FLDA1) and an Fe-starvation induced protein (ISIP3) as indicators of Fe limitation in the marine diatom Thalassiosira oceanica. The specificity of the response to Fe limitation was tested in cultures grown under Fe- and macronutrient-deficient conditions, as well as t ...[more]

PMID: 25333460

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Project description:There is an intricate interaction between iron (Fe) and copper (Cu) physiology in diatoms. However, strategies to cope with low Cu are largely unknown. This study unveils the comprehensive restructuring of the photosynthetic apparatus in the diatom Thalassiosira oceanica (CCMP1003) in response to low Cu, at the physiological and proteomic level. The restructuring results in a shift from light harvesting for photochemistry-and ultimately for carbon fixation-to photoprotection, reducing carbon fixation and oxygen evolution. The observed decreases in the physiological parameters Fv/Fm, carbon fixation, and oxygen evolution, concomitant with increases in the antennae absorption cross section (σPSII), non-photochemical quenching (NPQ) and the conversion factor (φe:C/ηPSII) are in agreement with well documented cellular responses to low Fe. However, the underlying proteomic changes due to low Cu are very different from those elicited by low Fe. Low Cu induces a significant four-fold reduction in the Cu-containing photosynthetic electron carrier plastocyanin. The decrease in plastocyanin causes a bottleneck within the photosynthetic electron transport chain (ETC), ultimately leading to substantial stoichiometric changes. Namely, 2-fold reduction in both cytochrome b6f complex (cytb6f) and photosystem II (PSII), no change in the Fe-rich PSI and a 40- and 2-fold increase in proteins potentially involved in detoxification of reactive oxygen species (ferredoxin and ferredoxin:NADP+ reductase, respectively). Furthermore, we identify 48 light harvesting complex (LHC) proteins in the publicly available genome of T. oceanica and provide proteomic evidence for 33 of these. The change in the LHC composition within the antennae in response to low Cu underlines the shift from photochemistry to photoprotection in T. oceanica (CCMP1003). Interestingly, we also reveal very significant intra-specific strain differences. Another strain of T. oceanica (CCMP 1005) requires significantly higher Cu concentrations to sustain both its maximal and minimal growth rate compared to CCMP 1003. Under low Cu, CCMP 1005 decreases its growth rate, cell size, Chla and total protein per cell. We argue that the reduction in protein per cell is the main strategy to decrease its cellular Cu requirement, as none of the other parameters tested are affected. Differences between the two strains, as well as differences between the well documented responses to low Fe and those presented here in response to low Cu are discussed.

Project description:BackgroundInfection with the myxozoan parasite Parvicapsula pseudobranchicola causes disease in wild and farmed salmonids in Norway. In the northeast Pacific Ocean, the parasite has been reported in Pacific salmon Oncorhynchus spp. without evidence of disease. The objectives of the present study were to confirm the identity of P. pseudobranchicola in the Pacific, document its host and geographic ranges, and describe associated pathological changes.MethodsOcean-entry year wild pink salmon Oncorhynchus gorbuscha, chum salmon O. keta, Chinook salmon O. tshawytscha, coho salmon O. kisutch and sockeye salmon O. nerka were collected in summer and autumn surveys near Vancouver Island (VI) and from a winter survey in the Gulf of Alaska. Samples were also obtained from farmed Atlantic salmon Salmo salar and Chinook salmon near VI. Samples were analysed by qPCR and histology using conventional staining or in situ hybridisation. Parasite sequence was obtained from small subunit ribosomal RNA gene (SSU rDNA).ResultsIdentical 1525 base-pair SSU rDNA sequences from infected pink salmon, chum salmon and Chinook salmon shared 99.93% identity with a P. pseudobranchicola sequence from Norwegian Atlantic salmon. In autumn surveys, the prevalence was greatest in chum salmon (91.8%) and pink salmon (85.9%) and less so in Chinook salmon (68.8%) and sockeye salmon (8.3%). In farmed salmon, the prevalence was zero in Atlantic salmon (n = 967) and 41% in Chinook salmon (n = 118). Infections were preferentially sited in pseudobranch and visualised by in situ hybridisation. Heavy parasite burdens in all species of Pacific salmon were inconsistently associated with focal granulomatous pseudobranchitis.ConclusionsIn the northeast Pacific, widespread occurrence of P. pseudobranchicola in Pacific salmon together with its absence or sporadic occurrence in farmed Atlantic salmon differs from its epidemiology in Norway, despite similar pathological development in the pseudobranch. Consequences of the infections to the health of wild Pacific salmon, identity of the invertebrate host and the distribution and abundance of infective actinospores are unknown and remain high priorities for research.

Dataset Information

Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean.

Publications

Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean.

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