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Journal Articles - UP - MSI

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  • Tolerance of Fucus vesiculosus exposed to diesel water-accommodated fraction (WAF) and degradation of hydrocarbons by the associated bacteria
    Ryzhik, Inna; Pugovkin, Dmitriy; Makarov, Mikhail; Roleda, Michael Y.; Basova, Larisa; Voskoboynikov, Grigoriy (Elsevier BV, 2019-11)
    The viability and physiological state of brown macroalgae Fucus vesiculosus and its associated epiphytic bacteria exposed to diesel water-accommodated fraction (WAF), as well as the capacity of this association to deplete petroleum hydrocarbons (HCs) were experimentally tested. After a 6-day exposure treatment, the algal-surface associated bacteria were identified as primarily hydrocarbon-oxidising bacteria (HOB), and the algal-HOB association was able to deplete petroleum hydrocarbons from the diesel WAF by 80%. The HOB density on the algal surface exposed to diesel WAF was 350% higher compared to the control (i.e. HOB density on the algal surface exposed to ambient seawater), which suggest that they actively proliferated in the presence of hydrocarbons and most likely consumed hydrocarbons as their primary organic substrate. Exposure to diesel WAF did not affect the metabolic activity of F. vesiculosus. Higher lipid peroxidation was observed in F. vesiculosus exposed to diesel WAF while catalase concentration decreased only during the first day of exposure. Results suggest F. vesiculosus is tolerant to oil pollution and the algal-HOB association can efficiently deplete petroleum hydrocarbons in oil-contaminated seas.
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    Microscopic stages of North Atlantic Laminaria digitata (Phaeophyceae) exhibit trait-dependent thermal adaptation along latitudes
    Schimpf, Nele M.; Liesner, Daniel; Franke, Kiara; Roleda, Michael Y.; Bartsch, Inka (Frontiers Media SA, 2022-06-17)
    Kelp forests in the North Atlantic are at risk of decline at their warm temperature distribution margins due to anthropogenic temperature rise and more frequent marine heat waves. To investigate the thermal adaptation of the cold-temperate kelp Laminaria digitata, we sampled six populations, from the Arctic to Brittany (Spitsbergen, Tromsø, Bodø [all Norway], Helgoland [Germany], Roscoff and Quiberon [both France]), across the species’ entire distribution range, spanning 31.5° latitude and 12-13°C difference in mean summer sea surface temperature. We used pooled vegetative gametophytes derived from several sporophytes to approximate the genetic diversity of each location. Gametophytes were exposed to (sub-) lethal high (20-25°C) and (sub-) optimal low (0-15°C) temperature gradients in two full-factorial, common-garden experiments, subjecting subsets of populations from different origins to the same conditions. We assessed survival of gametophytes, their ability to develop microscopic sporophytes, and subsequent growth. We hypothesized that the thermal performance of gametophytes and microscopic sporophytes corresponds to their local long-term thermal history. Integrated gametophyte survival revealed a uniform upper survival temperature (UST) of 24°C among five tested populations (Tromsø to Quiberon). In contrast, following two weeks of thermal priming of gametophytes at 20-22°C, sporophyte formation at 15°C was significantly higher in southern populations (Quiberon and Roscoff) compared to the high-latitude population of Tromsø. Between 0-15°C, survival of the Arctic population (Spitsbergen) was negatively correlated with increasing temperatures, while the southern-most population (Quiberon) showed the opposite. Thus, responses of survival at low, and sporophyte formation at high temperatures, support the concept of local adaption. On the other hand, sporophyte formation between 0-15°C peaked at 6-9°C in the Quiberon and at 9-12°C in the Spitsbergen population. Sporophyte growth rates (GR) both in length and width were similar for Spitsbergen, Tromsø and Quiberon; all had maximum GRs at 12-15°C and low GRs at 0-6°C. Therefore, responses of sporophyte formation and growth at low temperatures do not reflect ecotypic adaptation. We conclude that L. digitata populations display trait-dependent adaptation, partly corresponding to their local temperature histories and partly manifesting uniform or unpredictable responses. This suggests differential selection pressures on the ontogenetic development of kelps such as L. digitata.
    We would like to thank A. Wagner for the sampling and clonal isolation of kelp material and technical assistance in the laboratory, C. Daniel for support with the image analysis, L. Foqueau for the SST data, C. Gauci for statistical advice and S. DeAmicis for supervision in this BSc Thesis.
  • Enrichment of the protein content of the macroalgae Saccharina latissima and Palmaria palmata
    Aasen, Inga Marie; Sandbakken, Ingrid S.; Toldnes, Bendik; Roleda, Michael Y.; Slizyte, Rasa (Elsevier, 2022-06)
    The large brown seaweeds (kelps) are potential sources of protein for animal feed. They have lower protein contents than most red and green algae, but due to potential for large-scale production, they may represent a significant future protein source. The impact of pH, temperature and polysaccharide-degrading enzymes on the solubility and extraction yields of protein from wet Saccharina latissima biomass was investigated. The protein solubility increased with increasing pH and reached maximum of 23% at pH 11, determined as total amino acids (TAA). The enzyme treatments increased the release of soluble compounds by 30–35%. The highest protein yield obtained was 19%, using a ratio of water to wet seaweed of 1:1 for extraction. Even if the yields can be increased by increasing the water amounts used for extraction, the majority of the protein would remain in the insoluble residue after separation. The strategy for production of a larger quantity of protein-enriched biomass was therefore to maintain the insoluble fraction as the product. A pilot scale production was carried out, also including the red algae Palmaria palmata. In total 750 kg S. latissima and 195 kg P. palmata were processed. The protein content in the product increased from 10 to 20% of dry weight (dw) for S. latissima and from 12 to 28% for P. palmata, with yields of 79 and 69%, respectively. The ash content was reduced from 44 to 26% and from 12 to 5% of dw, respectively, for the two species. The main protein loss was free amino acids, which constituted approximately 10% of TAA in the feedstocks. Less essential than non-essential amino acids were lost, thus, the essential amino acids were enriched in the product.
    The work was funded by The Research Council of Norway, grant no. 244244.
  • Reproductive phenology and morphology of Macrocystis pyrifera (Laminariales, Ochrophyta) from southern New Zealand in relation to wave exposure1
    Leal, Pablo P.; Roleda, Michael Y.; Fernández, Pamela A.; Nitschke, Udo; Hurd, Catriona L. (Wiley, 2021-07-23)
    Macrocystis pyrifera is a major habitat forming kelp in coastal ecosystems of temperate regions of the northern and southern hemispheres. We investigated the seasonal occurrence of adult sporophytes, morphological characteristics, and reproductive phenology at two sites within a wave-protected harbour and two wave-exposed sites in southern New Zealand every 3–4 months between 2012 and 2013. Seasonality in reproduction was assessed via the number of sporophylls, the occurrence of sori on sporophylls, and non-sporophyllous laminae (fertile pneumatocyst-bearing blades and fertile apical scimitars), meiospore release, and germination. We found that M. pyrifera was present and reproductive year-round in three of the four sites, and patterns were similar for the wave-exposure conditions. Sori were found on pneumatocyst-bearing blades and apical scimitars in addition to the sporophylls, and viable meiospores were released from all three types of laminae. Morphological variations between sites with different wave exposure indicate that sporophytes from wave-protected sites have bigger blades and holdfasts and are longer than those from wave-exposed sites. We discuss the implications of these biological variables for the ecology of M. pyrifera inhabiting different wave exposure environments in southern New Zealand.
    Pablo P. Leal was supported by a scholarship from BECAS CHILE-ANID and by Programa Integral de Desarrollo de Acuicultura de Algas para Pescadores Artesanales (Etapa 4), funded by the Subsecretarıa de Economıa y Empresas de Menor Tamano (Convenio 2016). Michael Y. Roleda acknowledges the Philippine’s Department of Science and Technology (DOST) Balik Scientist Program for the fellowship. Udo Nitschke gratefully acknowledges support by Skidmore College, 815 North Broadway, Saratoga Springs, NY 12866, USA. Pamela A. Fernandez was supported by the Chilean National Commission for Scientific and Technological Research (ANID/FONDECYT; Postdoctoral grant 3170225 and grant 1180647) and ANID/Programa Basal (CeBiB, FB-0001). We are grateful to Rocio Suarez for assisting in field sampling.
  • Growth, nitrate uptake kinetics, and biofiltration potential of eucheumatoids with different thallus morphologies
    Narvarte, Bienson Ceasar V.; Genovia, Tom Gerald T.; Hinaloc, Lourie Ann R.; Roleda, Michael Y. (Wiley, 2021-12-30)
    The declining production of commercially important eucheumatoids related to serious problems like increasing susceptibility to ice‐ice disease and epiphytism may be ameliorated by nutrition. This ushered to an increasing interest in incorporating seaweeds into an integrated multi‐trophic aquaculture (IMTA) setup to take up excess inorganic nutrients produced by fish farms for their nourishment. In this regard, it is important to understand the nutrient uptake capacity of candidate seaweeds for incorporation in an IMTA system. Here, we examined the growth, nitrate (NO3‐) uptake kinetics and biofiltration potential of Eucheuma denticulatum and three strains of Kappaphycus alvarezii (G‐O2, TR‐C16 and SW‐13) with distinct thallus morphologies. The NO3‐ uptake rates of the samples were determined under a range of NO3‐ concentration (1‐ 48 µM) and uptake rates were fitted to the Michaelis‐Menten saturation equation. Among the examined eucheumatoids, only SW‐13 had a linear response to NO3‐ concentration while other strains had uptake rates that followed the Michaelis‐Menten saturation equation. Eucheuma denticulatum had the lowest Km (9.78 ± 1.48 µM) while G‐O2 had the highest Vmax (307 ± 79.3 µmol · g‐1 · min‐1). The efficiency in NO3‐ uptake (highest Vmax/Km and α) was translated into the highest growth rate (3.41± 0.58 % · d‐1) measured in E. denticulatum. Our study provided evidence that eucheumatoids could potentially take up large amount of NO3‐ and fix CO2 when cultivated proximate to a fish farm as one component of an IMTA system. During a 45‐d cultivation period of eucheumatoids, as much as 370 g NO3‐ can be sequestered by every 1 kg initial biomass E. denticulatum growing at 3% · d‐1. Furthermore, based on our unpublished photosynthetic measurements, the congeneric K. striatus can fix 27.5 g C · kg‐1 DW during a 12‐h daylight period.
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    The complete mitochondrial genome of a wild-collected Kappaphycus malesianus (Solieriaceae, Rhodophyta)
    Crisostomo, Bea A.; Dumilag, Richard V.; Roleda, Michael Y.; Lluisma, Arturo O. (Taylor & Francis, 2023-03-04)
    Kappaphycus malesianus is a red seaweed farmed primarily for its carrageenan, a polysaccharide important in the food and pharmaceutical industries. Among the commercially cultivated Kappaphycus species, only K. malesianus has no mitogenome data available. Here, we assembled the mitochondrial genome of K. malesianus from next-generation sequencing data. The circular mitogenome consisted of 25,250 base pairs (bp) with a GC content of 30.25%. These values were comparable to previously sequenced solieriacean mitogenomes. Structural features, such as the stem-loop and hairpin, which were previously reported in other rhodophytes mitochondrial DNA, were also identified. The annotated genes (24 protein-coding genes, 24 tRNA genes, and 2 rRNA genes) were arranged in an order similar to the other available solieriacean mitogenomes. Lastly, phylogenetic analysis using 23 predicted protein domains showed the sister relationship of K. malesianus with other Kappaphycus species.
    The authors are grateful to Z.-Z. Aguinaldo, S. Damsik, and J. Turong for aiding during laboratory and field works. The authors also acknowledge the LGU of Sitangkai, Tawi-Tawi for granting permission for the collection activities. This is contribution no. 495 from the University of the Philippines the Marine Science Institute (UPMSI), Diliman, Quezon City.
  • Short-term exposure to independent and combined acidification and warming elicits differential responses from two tropical seagrass-associated invertebrate grazers
    Baure, Jerwin G.; Roleda, Michael Y.; Juinio-Meñez, Marie Antonette (Springer, 2023-08-10)
    Ocean acidification and warming could affect animal physiology, key trophic interactions and ecosystem functioning in the long term. This study investigates the effects of four pH−temperature combination treatments simulating ocean acidification (OA), ocean warming (OW) and combined OA and OW conditions (FUTURE) relative to ambient present-day conditions (PRESENT) on the grazing of the juveniles of two seagrass-associated invertebrates namely the sea cucumber Stichopus cf. horrens and topshell Trochus maculatus over a 5-day exposure period. Diel and feeding activity of both species increased under OW and FUTURE to some extent, while the nighttime activity of Trochus but not Stichopus decreased under OA relative to PRESENT during the first 2 days. Fecal production of Stichopus did not differ among treatments, while the lowest fecal production of Trochus was observed under OA during the first 24 h of grazing. These responses suggest that Trochus may be initially more sensitive to OA compared with Stichopus. Interestingly, fecal production of Trochus in FUTURE was significantly higher than OA, suggesting that warming may ameliorate the negative effect of acidification. Diel activity, feeding and fecal production after 5 days did not differ among treatments for both species, suggesting acclimation to the acute changes in temperature and pH after a few days, although Stichopus acclimated rapidly than Trochus. The ability of the two juvenile invertebrate grazers to rapidly acclimate to increased temperature and lowered pH conditions after short-term exposure may favor their survival under projected changes in ocean conditions.
    This work was supported by the Department of Science and Technology–Philippine Council for Agriculture, Aquatic, and Natural Resources Research and Development under Grant QMSR-MRRD-MEC-295-1449. The authors would like to thank Dr. Ian Enochs for his invaluable help in improving this paper. We also thank Tirso Catbagan, Garry Bucol, Rona Soy and Tomilyn Jan Garpa for their assistance during the conduct of this study. We would also like to thank the Marine Biogeochemistry Laboratory of the UP Marine Science Institute for their assistance in analyzing our water samples as well as the DNA Barcoding Laboratory of the UP Institute of Biology for the species identification of our animals.
  • Genetic diversity of Kappaphycus malesianus (Solieriaceae, Rhodophyta) from the Philippines
    Dumilag, Richard V.; Crisostomo, Bea A.; Aguinaldo, Zae-Zae A.; Lluisma, Arturo O.; Gachon, Claire M.M.; Roleda, Michael Y. (Elsevier, 2023-07)
    Kappaphycus farming for carrageenan production is characterized by a strong selective pressure at the genetic level. Traits of agronomic importance are compromised due to domestication bottlenecks and the subsequent events of possible selective breeding of founding cultivars. Kappaphycus malesianus is farmed in Malaysia and the Philippines, and is distributed within the Malesian region. While the majority of genetically characterized specimens of this species are from Malaysia, those from the Philippines are poorly explored. Here, we assessed the genetic diversity of K. malesianus from the Philippines based on cox1 sequences. Of the 15 identified haplotypes, 14 specimens represent three novel haplotypes (wild specimens) that form a group distinct from the main clade comprising most K. malesianus haplotypes known to date. An additional haplotype from a cultivated specimen was identical to that of the most widely distributed haplotype. Our findings demonstrate that the K. malesianus is genetically more diverse than previously recognized. It is expected that higher genetic diversity may be revealed through additional sampling from a wider geographic range and careful application of integrative approaches. Future selective breeding programs in Kappaphycus would benefit from the incorporation of the genetic resources, as provided in this study.
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    Impacts of aquaculture nutrient sources: ammonium uptake of commercially important eucheumatoids depends on phosphate levels
    Narvarte, Bienson Ceasar V.; Hinaloc, Lourie Ann R.; Gonzaga, Shienna Mae C.; Roleda, Michael Y. (Springer, 2023-09-14)
    In an integrated multitrophic aquaculture (IMTA) system, seaweeds serve as extractive species that utilize excess nutrients, thereby reducing the risk of eutrophication and promoting sustainable aquaculture. However, the use of excessive fish feeds and the resultant faecal waste as nutrient streams can contribute to variations in nitrogen and phosphorus levels (e.g., primarily NH4+ and PO4−3) in the surrounding area and this may impact the physiology of the integrated seaweeds, particularly on how these species take up inorganic nutrients. In this study, the effect of different PO4−3 levels on NH4+ uptake of the three commercially important eucheumatoids Kappaphycus alvarezii, Kappaphycus striatus and Eucheuma denticulatum was examined under laboratory conditions. Seaweed thalli (n = 4) were incubated in seawater media containing 30 µM NH4+, and 0, 0.5, 1.0, 1.5, 3.0 or 5.0 µM PO4−3 for 1 h under a saturating light level of 116 ± 7.13 µmol photons m−2 s−1 inside a temperature-controlled laboratory. Species-specific responses to PO4−3 levels were observed. For K. alvarezii, maximum NH4+ uptake (17.8 ± 1.6 µmol gDW−1 h−1) was observed at 0.5 µM PO4−3 and the uptake rate declined at higher PO4−3 levels. For K. striatus, NH4+ uptake increased with increasing PO4−3 levels, with maximum N uptake (6.35 ± 0.9 µmol gDW−1 h−1) observed at 5.0 µM PO4−3. For E. denticulatum, maximum NH4+ uptake (14.6 ± 1.4 µmol gDW−1 h−1) was observed at 1.0 µM PO4−3. Our results suggest that among the three eucheumatoid species, the NH4+ uptake of K. striatus persists even at high levels of PO4−3. However, our results also showed that K. striatus had the lowest range of NH4+ uptake rates. These results should be taken into consideration when incorporating eucheumatoids in the IMTA system, where PO4−3levels significantly vary in space and time.
    This is contribution no. 500 from the Marine Science Institute, University of the Philippines (UPMSI), Diliman. The AlgaE Team would like to thank the Bolinao Marine Laboratory (BML) for providing the venue to conduct our experiments. BCV Narvarte and MY Roleda acknowledge the Sea6 Energy Pvt. Ltd. for sponsorship during the 24th International Seaweed Symposium (ISS) held on February 19-24, 2023, at Hobart, Tasmania, Australia. Likewise, BCV Narvarte and LAR Hinaloc would like to thank the University of the Philippines- Office of the International Linkages (UP-OIL) for providing them with a travel grant to attend the aforementioned symposium. BCV Narvarte also acknowledges the Department of Science and Technology- Philippine Council for Agriculture, Aquatic, and Natural Resources Research and Development (DOST-PCAARRD) for his PhD Scholarship (GREAT- Graduate Research and Education Assistantship for Technology Program).
  • Total polyphenol content of tropical marine and coastal flora: Potentials for food and nutraceutical applications
    Narvarte, Bienson Ceasar V.; Genovia, Tom Gerald T.; Hinaloc, Lourie Ann R.; Gonzaga, Shienna Mae C.; Tabonda-Nabor, April Mae; Palecpec, Flora Maye R.; Dayao, Helen M.; Roleda, Michael Y. (Springer, 2023-07-08)
    The marine environment is abundant in natural products that are beneficial to humans. Among these compounds are the polyphenols produced by marine flora as secondary metabolites and used as a defense against stressful environmental conditions. Accordingly, recent pharmacological and biomedical studies showed that polyphenols from marine and coastal floras have several important bioactivities including antioxidant property. In this study, we measured the total polyphenol content (TPC) of 75 species of marine-associated flora. The TPC of their methanolic extracts was measured spectrophotometrically using the Folin-Ciocalteu assay and was expressed both as mg phloroglucinol equivalent per g of dry weight (mg PGE g−1 DW) and as mg gallic acid equivalent per g dry weight (mg GAE g−1 DW). The TPC values are higher when expressed in terms of GAE compared to PGE. Also, the mean TPC of tracheopytes (229 ± 43.0 mg PGE g−1 DW) was higher compared to the mean TPC of macroalgae (69.4 ± 9.59 mg PGE g−1 DW). For macroalgae, ochrophytes (97.9 ± 22.7 mg PGE g−1 DW) had the highest mean TPC followed by chlorophytes (80.0 ± 20.5 mg PGE g−1 DW) and rhodophytes (49.5 ± 8.60 mg PGE g−1 DW). Moreover, our study also showed that TPC varied between young and mature tissues, among different color morphotypes and different parts of the plants. Although the concentrations of total polyphenols varied among species, ages, strains and parts of the plant, our study showed that marine and coastal floras are rich sources of polyphenols that could be further examined for their biological activities and other applications in food industry.