The Influence of Host Specificity and Temperature on Bacterial Communities Associated with Sargassum (Phaeophyceae) Species.

Host-related microbiota are critically important for the adaptation/acclimation of hosts to changing environments, but how environmental factors and host characteristics shape the microbial communities remains largely unknown. We investigated the effects of temperature on habitat-forming macroalgae and their associated bacterial communities. Three Sargassum species (S. horneri, S. fusiforme, and S. thunbergii) and seawater samples were sampled in Gouqi Island, China, and these macroalgal samples were incubated at different temperatures (10, 20, and 27°C) for 7 d. Bacterial communities were identified from the 16S rRNA gene V3-V4 regions. The algae-associated bacterial communities of the field samples were significantly different from seawater, implying host specificity. During laboratory incubation, decreased physiological status (photosynthetic rate and oxidative stress response) was detected for all the species at 10°C, especially with regard to S. horneri and S. fusiforme. For each host, associated bacterial communities at 20 and 27°C clustered closely, and these were separated from samples at 10°C based on constrained PCoA analyses. Permutational multivariate analysis of variance revealed that algae-associated bacterial communities were more affected by host species (23.3%) than by temperature (2.48%) during laboratory incubation. The changes in bacterial community composition may be influenced by algae metabolites, which should be tested in a future study. These results further contribute to our understanding of algal microbiome changes in response to environmental changes.

Invasion-mediated effects on marine trophic interactions in a changing climate: positive feedbacks favour kelp persistence.

The interactive effects of ocean warming and invasive species are complex and remain a source of uncertainty for projecting future ecological change. Climate-mediated change to trophic interactions can have pervasive ecological consequences, but the role of invasion in mediating trophic effects is largely unstudied. Using manipulative experiments in replicated outdoor mesocosms, we reveal how near-future ocean warming and macrophyte invasion scenarios interactively impact gastropod grazing intensity and preference for consumption of foundation macroalgae ( Ecklonia radiata and Sargassum vestitum). Elevated water temperature increased the consumption of both macroalgae through greater grazing intensity. Given the documented decline of kelp ( E. radiata) growth at higher water temperatures, enhanced grazing could contribute to the shift from kelp-dominated to Sargassum-dominated reefs that is occurring at the low-latitude margins of kelp distribution. However, the presence of a native invader ( Caulerpa filiformis) was related to low consumption by the herbivores on dominant kelp at warmer temperatures. Thus, antagonistic effects between climate change and a range expanding species can favour kelp persistence in a warmer future. Introduction of species should, therefore, not automatically be considered unfavourable under climate change scenarios. Climatic changes are increasing the need for effective management actions to address the interactive effects of multiple stressors and their ecological consequences, rather than single threats in isolation.

Green and golden seaweed tides on the rise.

Sudden beaching of huge seaweed masses smother the coastline and form rotting piles on the shore. The number of reports of these events in previously unaffected areas has increased worldwide in recent years. These 'seaweed tides' can harm tourism-based economies, smother aquaculture operations or disrupt traditional artisanal fisheries. Coastal eutrophication is the obvious, ultimate explanation for the increase in seaweed biomass, but the proximate processes that are responsible for individual beaching events are complex and require dedicated study to develop effective mitigation strategies. Harvesting the macroalgae, a valuable raw material, before they beach could well be developed into an effective solution.

Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed.

Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral-seaweed-herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.

Effects of extraction methods for a new source of biostimulant from Sargassum horneri on the growth of economically important red algae, Neopyropia yezoensis.

Sargassum horneri is a major bloom forming species in Korea and China. It is important to find a way to utilize the huge biomass of Sargassum horneri in the region. Seaweed-derived biostimulants are primarily derived from brown algae and are known to improve terrestrial crop growth and tolerance to abiotic stresses. Neopyropia yezoensis is the most important seaweed cultured species in Korea, and research is required to increase heat resistance as a solution against climate change. In this study, various extraction methods were used to obtain Sargassum horneri extract, and it was applied to Neopyropia yezoensis to evaluate the effect on physiological activity. Metabolites of Sargassum horneri were extracted by using four different methods: boiling (SBE), soaking (SSE), autoclaving (SAE) and ethanol (SEE). The SBE, SSE and SAE derived extracts showed increased tolerance to high-temperature stress that had inhibited the growth of Neopyropia yezoensis, and show improved growth compared to the control group. The SBE and SSE extraction methods improved the content of phycobiliprotein, but also the SBE increased superoxide dismutase (SOD) activity. Based on the results of this study, the boiling extraction method appears to be the most suitable method for the extraction of plants stimulants from Sargassum horneri.

Evaluation of the effect of Lactiplantibacillus pentosus SN001 fermentation on arsenic accumulation and antihypertensive effect of Sargassum horneri in vivo.

Sargassum horneri contains water-soluble polysaccharides, which have antihypertensive effects, and arsenic, which is harmful to the human body. Boiling and other treatments are effective in removing arsenic; however, water-soluble polysaccharides are lost during processing. Therefore, a method to remove arsenic and further increase its antihypertensive effect is required. To this end, we investigated fermentation with Lactiplantibacillus pentosus SN001 in this study. Boiled and fermented S. horneri were administered to spontaneously hypertensive rats (SHR), and blood pressure and arsenic accumulation in organs were observed to simultaneously examine the effects of fermentation on hypertension and arsenic accumulation. The ACE (angiotensin-converting enzyme) inhibition rate, an indicator of antihypertensive effects, showed a maximum at 4 days of fermentation. Consecutive dosing studies using S. horneri, boiled S. horneri, and fermented boiled S. horneri in SHR were conducted. Although the boiled group showed high blood pressure values, the fermented boiled group showed lower blood pressure values than the boiled cohort. The amount of arsenic accumulated in the liver, kidney, and spleen of rats was significantly lower in the boiled and fermented boiled groups than that in the S. horneri group. This confirmed the arsenic removal effect of boiling pretreatment and the in vivo safety of fermented boiled S. horneri. These results suggest that fermentation of arsenic-free S. horneri with L. pentosus SN001 can enhance its antihypertensive effect in vivo. This is the first study to simultaneously examine the antihypertensive effect of fermentation of S. horneri and its effect on the arsenic accumulation in vivo.

Suppression of herbivory by macroalgal density: a critical feedback on coral reefs?

Coral reefs globally are in decline, with some reefs undergoing phase shifts from coral-dominance to degraded states dominated by large fleshy macroalgae. These shifts have been underpinned by the overharvesting of herbivorous fishes and represent a fundamental change in the physical structure of these reefs. Although the physical structure provided by corals is regarded as a key feature that facilitates herbivore activity, the influence of the physical structure of macroalgal stands is largely unknown. Using transplanted Sargassum, the largest coral reef macroalga, we created habitat patches of predetermined macroalgal density (0.25-6.23 kg m(-2)). Remote video cameras revealed both grazing and browsing fishes avoided high density patches, preferring relatively open areas with low macroalgal cover. This behaviour may provide a positive feedback leading to the growth and persistence of macroalgal stands; increasing the stability of phase shifts to macroalgae.

Heatwaves during low tide are critical for the physiological performance of intertidal macroalgae under global warming scenarios.

The abundance and distribution of intertidal canopy-forming macroalgae are threatened by the increase in sea surface temperature and in the frequency and intensity of heatwaves caused by global warming. This study evaluated the physiological response of predominant intertidal macroalgae in the NW Iberian Peninsula (Bifurcaria bifurcata, Cystoseira tamariscifolia and Codium tomentosum) to increased seawater temperature during immersion and increased air temperatures during consecutive emersion cycles. We combined field mensuration and laboratory experiments in which we measured mortality, growth, maximum quantum yield and C:N content of the macroalgae. Air temperature was a critical factor in determining physiological responses and survivorship of all species, whereas high seawater temperature had sublethal effects. Cystoseira tamariscifolia suffered the greatest decreases in Fv/Fm, growth and the highest mortality under higher air temperatures, whereas C. tomentosum was the most resistant and resilient species. Two consecutive cycles of emersion under atmospheric heatwaves caused cumulative stress in all three macroalgae, affecting the physiological performance and increasing the mortality. The potential expansion of the warm-temperate species B. bifurcata, C. tamariscifolia and C. tomentosum in the NW Iberian Peninsula in response to increasing seawater temperature may be affected by the impact of increased air temperature, especially in a region where the incidence of atmospheric heatwaves is expected to increase.

Ocean acidification affects biological activities of seaweeds: A case study of Sargassum vulgare from Ischia volcanic CO2 vents.

We utilized volcanic CO2 vents at Castello Aragonese off Ischia Island as a natural laboratory to investigate the effect of lowered pH/elevated CO2 on the bioactivities of extracts from fleshy brown algae Sargassum vulgare C. Agardh. We analysed the carbohydrate levels, antioxidant capacity, antibacterial, antifungal, antiprotozoal, anticancer properties and antimutagenic potential of the algae growing at the acidified site (pH âˆ¼ 6.7) and those of algae growing at the nearby control site Lacco Ameno (pH∼8.1). The results of the present study show that the levels of polysaccharides fucoidan and alginate were higher in the algal population at acidified site. In general, extracts for the algal population from the acidified site showed a higher antioxidant capacity, antilipidperoxidation, antibacterial, antifungal, antiprotozoal, anticancer activities and antimutagenic potential compared to the control population. The increased bioactivity in acidified population could be due to elevated levels of bioactive compounds of algae and/or associated microbial communities. In this snapshot study, we performed bioactivity assays but did not characterize the chemistry and source of presumptive bioactive compounds. Nevertheless, the observed improvement in the medicinal properties of S. vulgare in the acidified oceans provides a promising basis for future marine drug discovery.

Effects of the brown algae Sargassum horneri and Saccharina japonica on survival, growth and resistance of small sea urchins Strongylocentrotus intermedius.

Mass mortality of the long line culture of the sea urchin Strongylocentrotus intermedius in summer, which is greatly associated with their disease, energy storage and resistant abilities, is the most serious problem for the development of the aquaculture. Here, a feeding experiment was conducted for ~ 9 weeks to investigate the survival, growth and gonadal development of small S. intermedius (~ 3 cm) fed either brown algae Sargassum horneri or Saccharina japonica. Subsequently, we assessed their resistant abilities via observing the behaviors of righting, tube feet extension and Aristotle's lantern reflex at both moderately elevated and acutely changed water temperatures. Sea urchins fed S. horneri showed significantly fewer diseased individuals and slower gonadal development than those fed S. japonica. Consistently, significantly greater Aristotle's lantern reflex occurred in sea urchins fed S. horneri at moderately elevated temperatures. These findings suggest that S. horneri has direct application potential as food for the long line culture of S. intermedius in summer because of the advantage in health, energy storage (avoid the energy loss caused by gonadal development at small body sizes) and resistance abilities. In comparison, sea urchins fed S. japonica outperformed those fed S. horneri for all experimental behaviors under the acutely changed water temperatures. These findings clearly suggest that S. intermedius fed S. japonica is more suitable for the areas with cold water mass in summer, because it can effectively avoid or reduce the negative impacts of acute changes of water temperature on sea urchins. The present study provides valuable information into the management of the long line culture of S. intermedius in summer.

Warming strengthens an herbivore-plant interaction.

Temperature has strong, predictable effects on metabolism. Through this mechanism, environmental temperature affects individuals and populations of poikilotherms by determining rates of resource use, growth, reproduction, and mortality. Predictable variation in metabolic processes such as growth and reproduction could affect the strength of species interactions, but the community-level consequences of metabolic temperature dependence are virtually unexplored. I experimentally tested the hypothesis that plant-herbivore interaction strength increases with temperature using a common species of marine macroalga (Sargassum filipendula) and the grazing amphipod Ampithoe longimana. Increasing temperature increased per capita interaction strength in two independent experiments and reversed a positive effect of temperature on plant growth. Temperature did not alter palatability of plant tissue to herbivores or average herbivore feeding rate. A predictable effect of temperature on herbivore-plant interaction strength could provide key information toward understanding local food web responses to changing temperatures at different spatial and temporal scales. Efforts to extend the effects of physiological mechanisms to larger scale patterns, including projections of the ecological effects of climate change, must be expanded to include the effects of changing conditions on trophic interactions.

Limited impact of Sargassum muticum on native algal assemblages from rocky intertidal shores.

Invasive species represent a serious threat to natural ecosystems through a range of negative effects on native species in the region invaded. The invasive species Sargassum muticum has invaded several temperate regions worldwide including the Galician rocky shoreline (northwestern Spain) in Western Europe. The main aim of this study was to assess if colonization by S. muticum has any effect on native algal assemblages by experimental removal of S. muticum. We predicted that in those plots where S. muticum plants were removed, the structure of native algal assemblages would differ from that in plots where S. muticum plants were untouched. In addition, we predicted that the effect of Sargassum removal would be more important than other causes of variability at the small scale investigated. Results indicated limited impact of S. muticum on native assemblages. The impact was only evident on the total number of native taxa and two understory morpho-functional groups, filamentous and foliose algae, rather than on the entire macroalgal assemblages.

Effects of increased CO2 and temperature on the physiological characteristics of the golden tide blooming macroalgae Sargassum horneri in the Yellow Sea, China.

The golden tide, caused by the brown algae Sargassum horneri, exerts severe influences on the Pyropia aquaculture of Jiangsu coast, China. To study the outbreak of the golden tide in response to increasing greenhouse gas emissions, S. horneri was cultured under four conditions: ambient condition (10 °C, 400 µatm), elevated temperature condition (14 °C, 400 µatm), elevated CO2 level (10 °C, 1000 µatm), and potential greenhouse condition (14 °C, 1000 µatm). The growth, photosynthetic performances, and inorganic carbon affinity of S. horneri were studied. The results showed that elevated temperature exerted a more pronounced positive influence on S. horneri growth, photosynthesis, and carbon assimilation than CO2 enrichment. The growth of S. horneri was significantly improved by moderately elevated temperatures, especially under concurrently elevated CO2 levels. This suggests that the greenhouse effect will benefit growth and carbon sequestration of S. horneri, which may enhance the frequency and scale of golden tides.

Environmental heterogeneity mediates scale-dependent declines in kelp diversity on intertidal rocky shores.

Biodiversity loss is driven by interacting factors operating at different spatial scales. Yet, there remains uncertainty as to how fine-scale environmental conditions mediate biological responses to broad-scale stressors. We surveyed intertidal rocky shore kelp beds situated across a local gradient of wave action and evaluated changes in kelp diversity and abundance after more than two decades of broad scale stressors, most notably the 2013-2016 heat wave. Across all sites, species were less abundant on average in 2017 and 2018 than during 1993-1995 but changes in kelp diversity were dependent on wave exposure, with wave exposed habitats remaining stable and wave sheltered habitats experiencing near complete losses of kelp diversity. In this way, wave exposed sites have acted as refugia, maintaining regional kelp diversity despite widespread local declines. Fucoids, seagrasses and two stress-tolerant kelp species (Saccharina sessilis, Egregia menziesii) did not decline as observed in other kelps, and the invasive species Sargassum muticum increased significantly at wave sheltered sites. Long-term monitoring data from a centrally-located moderate site suggest that kelp communities were negatively impacted by the recent heatwave which may have driven observed losses throughout the region. Wave-sheltered shores, which saw the largest declines, are a very common habitat type in the Northeast Pacific and may be especially sensitive to losses in kelp diversity and abundance, with potential consequences for coastal productivity. Our findings highlight the importance of fine-scale environmental heterogeneity in mediating biological responses and demonstrate how incorporating differences between habitat patches can be essential to capturing scale-dependent biodiversity loss across the landscape.

What nutrient sources support anomalous growth and the recent sargassum mass stranding on Caribbean beaches? A review.

Since 2011, tropical beaches from Africa to Brazil, Central America, and the Caribbean have been inundated by tons of sargassum seaweed from a new equatorial source of pelagic sargassum in the Atlantic. In recent years the extraordinary accumulations of sargassum make this a nuisance algal bloom for tropical coasts. In 2018 satellite data indicated floating mats of sargassum that extended throughout the Caribbean to the northeast coast of Brazil with the highest percent coverage over the water yet recorded. A literature review suggests that Atlantic equatorial recirculation of seaweed mats combined with nutrients from several possible sources may be stimulating the growth and accumulations of sargassum. In the western equatorial recirculation area, new nutrient sources may include Amazon River floods and hurricanes; in the eastern equatorial recirculation area, nutrient sources that could sustain the sargassum blooms include coastal upwelling and Congo River freshwater and nutrients.

Removal of an established invader can change gross primary production of native macroalgae and alter carbon flow in intertidal rock pools.

The impact of invasive species on recipient communities can vary with environmental context and across levels of biological complexity. We investigated how an established invasive seaweed species affected the biomass, eco-physiology, carbon and nitrogen storage capacity of native seaweeds at sites with a different environmental setting due to a persistent upwelling in northern Spain. We removed the invasive Japanese wireweed Sargassum muticum from intertidal rock pools once every month during a one-year period and used an in-situ stable isotope pulse-chase labeling to estimate gross primary production (GPP), nitrogen uptake rate, 13C-carbon and 15N-nitrogen storage capacities. Following the addition of 13C-enriched bicarbonate and 15N-enriched nitrate to the seawater in the rock pools during the period of the low tide, we sampled macroalgal thalli at incoming tide to determine label uptake rate. After four days, we sampled macroalgal assemblages to determine both label storage capacity and biomass. After one year of removal there was no change in the macroalgal assemblage. However, both the GPP and 13C-carbon storage capacity were higher in the turf-forming Corallina spp. and, sometimes, in the canopy-forming Bifurcaria bifurcata. Nitrogen uptake rate followed similar, but more variable results. Although S. muticum inhibited carbon storage capacity of native species, the assemblage-level 13C-carbon storage was similar in the S. muticum-removed and control rock pools because the presence of the invasive species compensated for the functional loss of native species, particularly at sites where it was most abundant. No obvious effects were observed in relation to the environmental setting. Overall, the effect of the invasive S. muticum on carbon flow appeared to be mediated both by the effects on resource-use efficiency of native species and by its own biomass. Integrating physiological and assemblage-level responses can provide a broad understanding of how invasive species affect recipient communities and ecosystem functioning.

Faunal mortality associated with massive beaching and decomposition of pelagic Sargassum.

In 2018, the Mexican Caribbean coast received a massive influx of pelagic Sargassum spp. that accumulated and decayed on beaches producing organic decomposition products that made the water turbid and brown. Between May and September of the same year there were several reports of mass mortality of marine biota in this area. From these reports we estimate that organisms belonging to 78 faunal species died as result of this event, with demersal neritic fish and Crustacea being the most affected groups. The cause of mortality appears to be the combined effect of high ammonium and hydrogen sulfide concentrations, together with hypoxic conditions. If massive arrival of pelagic Sargassum spp. continues and algae is left to decay on the beach in large volumes then deterioration in water quality could affect coral reefs close to shore. Furthermore, barriers placed in lagoons to intercept the Sargassum spp. before it reaches the beach could impact reef fauna if the algae is left to die and sink on site.

Physiological damages of Sargassum cymosum and Hypnea pseudomusciformis exposed to trace metals from mining tailing.

The damages of Mariana's mining mud in the physiology of the brown algae Sargassum cymosum and its main epiphytic, the red algae Hypnea pseudomusciformis, were evaluated by controlled essays. Seaweeds were exposed to presence or absence of mud, isolated or in biological association, for 5 and 15 days. Measured parameters were growth rates, biochemical descriptors, and the chemical investigation of concentration and metal profile of the mud dissolved in seawater. Results showed that the highest values for metals were Al > Fe > Mn > Zn in both exposure periods. The mud also affected the growth rate with lethality in both isolated and associative treatments with H. pseudomusciformis after 15 days. According to our redundancy analysis (RDA), the profile and concentration of all metallic elements can induce different physiological responses of the organisms. We were able to observe a higher physiological adaptive ability of S. cymosum against the long-term presence of metals by the synthesis of phenolic compounds, while the deviation of metabolic routes in H. pseudomusciformis can be addressed as the main responsible for its lethality. Moreover, the presence of Hypnea in associative treatments reduces Sargassum's detoxification ability. The present results reinforce the importance of biological interaction studies in a context of physiological resilience against mining mud pollution and mutual influences of species over the individual ability to avoid oxidative stress.

Biosorption of hexavalent chromium onto raw and chemically modified Sargassum sp.

Hexavalent chromium biosorption by raw algae is always accompanied with significantly high organic leaching. In this study, hydrochloric acid, sodium hydroxide, calcium chloride, formaldehyde, and glutaraldehyde were used for modification of raw Sargassum sp. seaweed (RSW), in order that the modified seaweed (MSW) has a lower organic leaching while the metal biosorption capacity is comparable to the RSW. The result shows that the chemical modification by 0.2% formaldehyde achieves such goals. The biosorption of both RSW and MSW is highly pH dependent. At the optimal pH of 2.0, the maximum biosorption capacities of MSW and RSW are 1.123 and 0.601 mmol g(-1), respectively. The surface treatment improves the reduction capacity of the biosorbents. The instrumental analysis demonstrates that the Cr(VI) biosorption is controlled by redox, ion exchange and coordination reactions, of which alcohol, carboxyl, amino and sulphonic groups play important roles. The complete uptake of hexavalent chromium is achieved in 20 h. The chemical reduction for Cr(VI) to Cr(III) is pH dependent and controls the overall chromium removal kinetics.

Effects of ocean acidification on the levels of primary and secondary metabolites in the brown macroalga Sargassum vulgare at different time scales.

Most of the studies regarding the impact of ocean acidification on macroalgae have been carried out for short-term periods, in controlled laboratory conditions, thus hampering the possibility to scale up the effects on long-term. In the present study, the volcanic CO2 vents off Ischia Island were used as a natural laboratory to investigate the metabolic response of the brown alga Sargassum vulgare to acidification at different time scales. For long-term effects, algal populations naturally growing at acidified and control sites were compared. For short-term responses, in situ reciprocal transplants from control to acidified site and vice-versa were performed. Changes in the levels of sugars, fatty acids (FAs), amino acids (AAs), antioxidants, and phenolic compounds were examined. Our main finding includes variable metabolic response of this alga at different time scales to natural acidification. The levels of sugars, FAs, and some secondary metabolites were lower in the natural population at the acidified site, whereas the majority of AAs were higher than those detected in thalli growing at control site. Moreover, in algae transplanted from control to acidified site, soluble sugars (glucose and mannose), majority of AAs, and FAs increased in comparison to control plants transplanted within the same site. The differences in the response of the macroalga suggest that the metabolic changes observed in transplants may be due to acclimation that supports algae to cope with acidification, thus leading to adaptation to lowered pH in long time scale.