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Journal Articles - UP - MSI

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  • A unique reproductive strategy in the mushroom coral Fungia fungites
    Eyal-Shaham, Lee; Eyal, Gal; Ben-Zvi, Or; Sakai, Kazuhiko; Harii, Saki; Sinniger, Frederic; Hirose, Mamiko; Cabaitan, Patrick; Bronstein, Omri; Feldman, Bar; Shlesinger, Tom; Levy, Oren; Loya, Yossi (Springer Science and Business Media LLC, 2020-09-30)
    The vast majority of scleractinian corals are either simultaneous hermaphrodites or gonochoric. Exceptions to these are rare. Nevertheless, species belonging to the family Fungiidae are known to exhibit a wide variety of reproductive strategies. We examined the reproductive ecology of the mushroom coral Fungia fungites in Okinawa. Our study was conducted as part of a long-term, wide-ranging project (2009–2010 and 2013–2017) which explored the unique reproductive strategies of several species belonging to the family Fungiidae. Here we report the co-occurrence of males, females, and hermaphrodite individuals in a long-term monitored population of the reproductively atypical brooder coral F. fungites within the family Fungiidae. F. fungites status as a single-polyped solitary coral, was used to perform manipulative experiments to determine the degree of dependence of an individual coral on its conspecific neighbors for reproduction, and examined whether a constant sperm supply is obligatory for the continuous production of planulae. Isolated females of F. fungites exhibited a distinctive reproductive strategy, expressed in continuously releasing planulae also in the absence of males. Observations conducted on a daily basis for 2.5 months (throughout the reproductive season of 2015) revealed that some of these individuals released planulae continuously, often between tens and hundreds every day. In an effort to explain this phenomenon, three hypotheses are discussed: (1) Self-fertilization; (2) Asexual production of planulae (i.e., parthenogenetic larvae); and (3) Extended storage of sperm. Finally, we emphasize the importance of continuous and long-term monitoring of studies of coral reproduction; through further genetic studies of coral populations representing a broad range of species and their larval origin.
  • Bacterial community assembly, succession, and metabolic function during outdoor cultivation of Microchloropsis salina
    Morris, Megan M.; Kimbrel, Jeffrey A.; Geng, Haifeng; Tran-Gyamfi, Mary Bao; Yu, Eizadora T.; Sale, Kenneth L.; Lane, Todd W.; Mayali, Xavier (American Society for Microbiology, 2022-08-31)

    Outdoor cultivation of microalgae has promising potential for renewable bioenergy, but there is a knowledge gap on the structure and function of the algal microbiome that coinhabits these ecosystems. Here, we describe the assembly mechanisms, taxonomic structure, and metabolic potential of bacteria associated with Microchloropsis salina cultivated outdoors. Open mesocosms were inoculated with algal cultures that were either free of bacteria or coincubated with one of two different strains of alga-associated bacteria and were sampled across five time points taken over multiple harvesting rounds of a 40-day experiment. Using quantitative analyses of metagenome-assembled genomes (MAGs), we tracked bacterial community compositional abundance and taxon-specific functional capacity involved in algal-bacterial interactions. One of the inoculated bacteria (Alteromonas sp.) persisted and dispersed across mesocosms, whereas the other inoculated strain (Phaeobacter gallaeciensis) disappeared by day 17 while a taxonomically similar but functionally distinct Phaeobacter strain became established. The inoculated strains were less abundant than 6 numerically dominant newly recruited taxa with functional capacities for mutualistic or saprophytic lifestyles, suggesting a generalist approach to persistence. This includes a highly abundant unclassified Rhodobacteraceae species that fluctuated between 25% and 77% of the total community. Overall, we did not find evidence for priority effects exerted by the distinct inoculum conditions; all mesocosms converged with similar microbial community compositions by the end of the experiment. Instead, we infer that the 15 total populations were retained due to host selection, as they showed high metabolic potential for algal-bacterial interactions such as recycling alga-produced carbon and nitrogen and production of vitamins and secondary metabolites associated with algal growth and senescence, including B vitamins, tropodithietic acid, and roseobacticides.

    IMPORTANCE Bacteria proliferate in nutrient-rich aquatic environments, including engineered algal biofuel systems, where they remineralize photosynthates, exchange secondary metabolites with algae, and can influence system output of biomass or oil. Despite this, knowledge on the microbial ecology of algal cultivation systems is lacking, and the subject is worthy of investigation. Here, we used metagenomics to characterize the metabolic capacities of the predominant bacteria associated with the biofuel-relevant microalga Microchloropsis salina and to predict testable metabolic interactions between algae and manipulated communities of bacteria. We identified a previously undescribed and uncultivated organism that dominated the community. Collectively, the microbial community may interact with the alga in cultivation via exchange of secondary metabolites which could affect algal success, which we demonstrate as a possible outcome from controlled experiments with metabolically analogous isolates. These findings address the scalability of lab-based algal-bacterial interactions through to cultivation systems and more broadly provide a framework for empirical testing of genome-based metabolic predictions.

  • MPA-FishMApp – a citizen science app that simplifies monitoring of coral reef fish density and biomass in marine protected areas
    Abesamis, Rene; Balingit, Rodel; de Castro, Romulo; Aguila, Raphael Nelo; Cabiguin, Maryjune; Villagracia, Julius; Susmeña, Marynoll; Montemar, Mario Neil; Yocor, Antonio (National Fisheries Research and Development Institute, 2022-12)
    Monitoring changes in fish density and biomass inside marine protected areas (MPAs) through fish visual census (FVC) can determine if MPAs are achieving their goal of promoting fish population recovery. Simplified FVC methods have been developed for citizen scientists to enable them to monitor fish populations in MPAs. However, MPA monitoring programs led by local stakeholders remain rare and difficult to sustain due to technical barriers related to FVC data management. Here, we describe and evaluate a novel online app called MPA-FishMApp, which we developed to help stakeholders of MPAs that protect coral reefs in the Philippines efficiently store, analyze, and visualize FVC data. MPA-FishMApp is coupled to a simplified FVC method wherein the observer records only 21 reef fish species groups during surveys. The app provides a simple data entry interface, cloud storage, and algorithms to estimate fish density and biomass. Spatial and temporal trends in fish density and biomass can be instantaneously visualized in the app based on relative importance to fisheries. Field testing suggested that the MPA-FishMApp methodology (simplified FVC and app) is sensitive enough to detect qualitative patterns showing differences in density and biomass that may develop between MPAs and fished sites, especially in fishes that are highly important to fisheries. However, users must have sufficient training and experience in simplified FVC to produce reliable data. MPA-FishMApp may help reverse the lack of monitoring in MPAs across the Philippines and offers an accessible, transparent, and auditable venue for collaboration between citizen scientists and professional scientists.
  • A conserved biosynthetic gene cluster is regulated by quorum sensing in a shipworm symbiont
    Robes, Jose Miguel D.; Altamia, Marvin A.; Murdock, Ethan G.; Concepcion, Gisela; Haygood, Margo G.; Puri, Aaron W. (American Society for Microbiology, 2022-06-14)
    Bacterial symbionts often provide critical functions for their hosts. For example, wood-boring bivalves called shipworms rely on cellulolytic endosymbionts for wood digestion. However, how the relationship between shipworms and their bacterial symbionts is formed and maintained remains unknown. Quorum sensing (QS) often plays an important role in regulating symbiotic relationships. We identified and characterized a QS system found in Teredinibacter sp. strain 2052S, a gill isolate of the wood-boring shipworm Bactronophorus cf. thoracites. We determined that 2052S produces the signal N-decanoyl-l-homoserine lactone (C10-HSL) and that this signal controls the activation of a biosynthetic gene cluster colocated in the symbiont genome that is conserved among all symbiotic Teredinibacter isolates. We subsequently identified extracellular metabolites associated with the QS regulon, including ones linked to the conserved biosynthetic gene cluster, using mass spectrometry-based molecular networking. Our results demonstrate that QS plays an important role in regulating secondary metabolism in this shipworm symbiont. This information provides a step toward deciphering the molecular details of the relationship between these symbionts and their hosts. Furthermore, because shipworm symbionts harbor vast yet underexplored biosynthetic potential, understanding how their secondary metabolism is regulated may aid future drug discovery efforts using these organisms.
  • Somatostatin venom analogs evolved by fish-hunting cone snails: From prey capture behavior to identifying drug leads
    Ramiro, Iris Bea L.; Bjørn-Yoshimoto, Walden E.; Imperial, Julita S.; Gajewiak, Joanna; Salcedo, Paula Flórez; Watkins, Maren; Taylor, Dylan; Resager, William; Ueberheide, Beatrix; Bräuner-Osborne, Hans; Whitby, Frank G.; Hill, Christopher P.; Martin, Laurent F.; Patwardhan, Amol; Concepcion, Gisela; Olivera, Baldomero M.; Safavi-Hemami, Helena (American Association for the Advancement of Science, 2022-03-25)
    Somatostatin (SS) is a peptide hormone with diverse physiological roles. By investigating a deep-water clade of fish-hunting cone snails, we show that predator-prey evolution has generated a diverse set of SS analogs, each optimized to elicit specific systemic physiological effects in prey. The increased metabolic stability, distinct SS receptor activation profiles, and chemical diversity of the venom analogs make them suitable leads for therapeutic application, including pain, cancer, and endocrine disorders. Our findings not only establish the existence of SS-like peptides in animal venoms but also serve as a model for the synergy gained from combining molecular phylogenetics and behavioral observations to optimize the discovery of natural products with biomedical potential.
  • C30 — A simple, rapid, scientifically valid, and low-cost method for citizen-scientists to monitor coral reefs
    Licuanan, Wilfredo Y.; Mordeno, Princess Zyrlyn B.; Go, Marco V. (Elsevier, 2021-09)
    The extent and speed of recent changes in reef coral abundances due to ocean warming and human impacts require more widespread capability to map and measure these changes, especially in countries like the Philippines. We present “C30”, a simple, rapid, scientifically valid, and low-cost method for skin divers or freedivers to take random photo-quadrat images within predefined stations on the upper reef slope. C30 yields coral cover data similar to those collected using the more intensive C5 method and can be as powerful in detecting small differences in reef cover. Less time is also needed for training personnel and sampling. However, more photo-quadrat images, better cameras, and closer collaboration with local scientists are required if higher precision data and estimates of coral diversity are needed from C30. C30 is a valuable tool for participatory, community-based citizen science monitoring of coral reefs.
    We thank the Department of Science and TechnologyPhilippine Council for Agriculture, Aquatic and Natural Resources Research and Development (QMSR-MRRD-COR-0-1209 and PCAARRD-GIA 4478), and the Department of Environment and Natural Resources Coral Reef Visualization and Assessment, The Philippines Project for funding some of the fieldwork. The initial research on citizen-science monitoring was undertaken with funding from Oscar M. Lopez Center for Climate Change Adaptation and Disaster Risk Management Foundation, Inc., The Philippines (Grant number OMLC RG 2017-18). We also thank the DLSU Innovation and Technology Office for the patent application for the C30 monopod in the Intellectual Property Office of the Philippines. The comments and suggestions of the reviewers are acknowledged and are very much appreciated. WY Licuanan is the holder of the Br H Alfred Shields FSC Professorial Chair in Biology and Br Cresentius Richard Duerr FSC Professorial Chair in Biochemistry.
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    Distribution, temporal change, and conservation status of tropical seagrass beds in Southeast Asia: 2000–2020
    Sudo, Kenji; Quiros, T. E. Angela L.; Prathep, Anchana; Luong, Cao Van; Lin, Hsing-Juh; Bujang, Japar Sidik; Ooi, Jillian Lean Sim; Fortes, Miguel D.; Zakaria, Muta Harah; Yaakub, Siti Maryam; Tan, Yi Mei; Huang, Xiaoping; Nakaoka, Masahiro (Frontiers Media SA, 2021-07-08)
    Although Southeast Asia is a hotspot of global seagrass diversity, there are considerable information gaps in the distribution of seagrass beds. Broad-scale seagrass distribution has not been updated in the global seagrass database by UNEP-WCMC since 2000, although studies on seagrasses have been undertaken intensively in each region. Here we analyze the recent distribution of tropical seagrass beds, their temporal changes, causes of decline and conservation status in Southeast Asia (plus southern mainland China, Taiwan and Ryukyu Island of Japan) using data collected after 2000. Based on the 195 literature published since 2000, we identified 1,259 point data and 1,461 polygon data showing the distribution of seagrass beds. A large discrepancy was found in the seagrass bed distribution between our updated data and the UNEP-WCMC database, mostly due to inaccurate and low resolution location information in the latter. Temporal changes in seagrass bed area analyzed for 68 sites in nine countries/regions demonstrated that more than 60% of seagrass beds declined at an average rate of 10.9% year–1, whereas 20% of beds increased at an average rate of 8.1% year–1, leading to an overall average decline of 4.7% year–1. Various types of human-induced threats were reported as causes for the decline, including coastal development, fisheries/aquaculture, and natural factors such as typhoons and tsunamis. The percentage of seagrass beds covered with existing marine protected areas (MPAs) varied greatly among countries/regions, from less than 1% in Brunei Darussalam and Singapore to 100% in southern Japan. However, the degree of conservation regulation was not sufficient even in regions with higher MPA coverage. The percentage of seagrass beds within EBSAs (Ecologically and Biologically Significant Area determined by the Convention of Biological Diversity) was higher than that within MPAs because EBSAs cover a greater area than MPAs. Therefore, designating EBSAs as legally effective MPAs can greatly improve the conservation status of seagrass beds in Southeast Asia.
    This manuscript is a contribution to the Asia-Pacific Marine Biodiversity Observation Network (AP-MBON) of the Group on Earth Observations Biodiversity Observation Network (GEO BON). We are grateful to the members of Phuket Marine Biological Center in Thailand and the Vietnam Academy of Science and Technology for providing local literature and data on seagrass bed distribution. This paper is dedicated to Chittima Aryuthaka who contributed greatly to the development of marine biology and ecology in Asia during her lifetime.
  • Dissolved and particulate carbon export from a tropical mangrove‐dominated riverine system
    Ray, Raghab; Miyajima, Toshihiro; Watanabe, Atsushi; Yoshikai, Masaya; Ferrera, Charissa M.; Orizar, Iris; Nakamura, Takashi; San Diego‐McGlone, Maria Lourdes; Herrera, Eugene C.; Nadaoka, Kazuo (Wiley, 2021-09-24)
    Despite being a major component in the mangrove carbon (blue carbon) budget, “outwelling” flux (or export to the sea) has gained little attention relative to other biogeochemical fluxes and reservoir carbon stock estimations. This study aims to estimate lateral exchange fluxes of dissolved and particulate organic carbon (DOC, POC) and dissolved inorganic carbon (DIC) from the watershed through a microtidal mangrove-dominated estuary to the coastal sea in Panay Island, Philippines. Along the estuarine transect, consistent addition of DOC, DIC, and POC at higher salinities were attributed to mangrove organic matter input. Upstream groundwater input (carbonate weathering) and downstream mangrove organic matter decomposition (possibly sulfate reduction) were the main controls on DIC. DOC corresponded to relatively pure mangrove sources in creek water, while POC was a mixture of detrital and algal organic matter. The mangrove system acted as net exporter of carbon to the sea in both dry and wet seasons. From short-term observations, outwelling fluxes of mangrove-derived DOC, DIC, and POC contributed 27–53%, 8–31%, and 42%, respectively, to their estuarine outflow. Unlike other studies, such low percentage for DIC might result from other external nonmangrove input (e.g., watershed carbonate weathering). Overall estuarine carbon flux was dominated by DIC (90–95%) with only minor contribution from DOC. The approach utilized in this study to estimate lateral carbon flux specific to a small mangrove setting can be useful in delineating blue carbon budgets that avoid geographical and methodological biases.
    We are grateful to the Japan International Cooperation Agency (JICA) and Japan Science and Technology Agency (JST) through the Science and Technology Research Partnership for Sustainable Development Program (SATREPS) for financially supporting the Project “Comprehensive Assessment and Conservation of Blue Carbon Ecosystems and their Services in the Coral Triangle (BlueCARES).” We are indebted to Dr Gerd Gleixner and Steffen Ruehlow (MPI-Jena, Germany) for providing support in δ13DOC analyses, and Dr Naoko Morimoto for POM analyses. We sincerely thank Dr Kenji Ono for sharing fine root production data. We are thankful to Dr Ariel Blanco (Department of Geodetic Engineering, UP Diliman) for providing delineation of mangrove area and Dr. Enrico C. Paringit, program leader of Phil-LiDAR 1, for providing the LiDAR products for map preparation. We thank Jeffrey Munar, Jesus Abad, John Michael Aguilar, Dominic Bautista, Bryan C. Hernandez and Mr Tsuyoshi Kanda for their assistance during field surveys. We are grateful for the overall support given by the University of the Philippines, Diliman and Aklan State University to the project. Finally, we thank the Journal Editor, Associate Editor, and three reviewers for their valuable comments and corrections on the manuscript.
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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.
  • Partial mortality in Porites corals: Variation among Philippine reefs
    Wesseling, Ineke; Uychiaoco, Andre J.; Aliño, Porfirio M.; Vermaat, Jan E. (Wiley, 2001-01)
    Partial mortality or tissue necrosis was quantified in the massive scleractinian coral Porites at three sites in The Philippines (Bolinao, NW Luzon; Puerto Galera, Mindoro; and El Nido, N Palawan). Overall, 15 ± 1 (mean ± 1 standard error, 642 replicates) percent of colony area was dead, mean colony area was 1135 plusmn; 127 cm2, and lesion density was 1.7 ± 0.1 dm—2. Total live coral cover varied between 20 and 63% in belt transects, and Porites and Acropora cover were inversely correlated. ANOVA models incorporating effects of site, colony size, sedimentation rates, wave exposure and depth were highly significant but explained only a small proportion of the variation observed in lesion density and percent dead area (respectively 8 and 2%). Lesion density was found to vary significantly with site (contributed 29% to this explained variance), decrease with increasing colony area (33%), and increase with increasing sedimentation (23%) and wave exposure (14%). Colony size was significantly explained by the factor site (contributing 61% to the total 29% explained variance) and depth (34%), with the smallest colonies being observed in Bolinao and the largest in El Nido. Densities of lesions were highest in Bolinao, intermediate in Puerto Galera, and lowest in El Nido. This pattern is parallel to intensity of human reef exploitation and opposite to that in colony size, live coral cover and Acropora cover. Since only a small part of the observed variance in partial mortality estimators was explained by the ANOVAs, other factors not quantified here must have been more important (e.g. disease incidence, predation, human exploitation).