Brown algae constitute key primary producers in cold and temperate coastal ecosystems, and face various stresses including pathogen infection. Yet the molecular mechanisms underlying their pathogen defence responses remain poorly understood. Here, we investigated the cell wall remodelling processes that define basal immunity in brown algae by comparing Ectocarpus strains with contrasting resistance levels to the biotrophic oomycete pathogen Eurychasma dicksonii. Using transmission electron microscopy, biochemical analyses, single-molecule fluorescent in situ hybridization (smFISH) and RNA sequencing, we demonstrate that infection triggers extensive extracellular matrix reorganization across all strain combinations. Resistant strains exhibited constitutively higher phlorotannin levels and increased physode abundance, while susceptible strains showed significant cell wall thickening and a less enhanced cell wall-bound phlorotannin accumulation following infection. Single-molecule FISH analysis demonstrated spatial recruitment of phlorotannin biosynthesis (polyketide synthase) and crosslinking (vanadium-dependent bromoperoxidase) transcripts to infection sites, forming characteristic ring-like patterns around infection areas. Transcriptomic analysis revealed extensive remodelling of cell wall biosynthetic pathways, with particular emphasis on genes encoding carbohydrate-active enzymes and Wall Sensing Component (WSC) domain proteins. These findings establish a molecular and biochemical framework of brown algal basal immunity, highlighting extracellular matrix remodelling as a conserved defence strategy against biotrophic oomycetes.
Epiphytic pests represent a persistent constraint on seaweed aquaculture, yet their temporal dynamics and system-specific impacts remain poorly quantified for many commercially important species. In southern Chile, cultivation of the agarophyte Gracilaria chilensis is increasingly affected by recurrent pest outbreaks, contributing to production instability and yield decline. Here, we conducted a replicated, multi-season field experiment across five cultivation setups (intertidal and subtidal long-lines and sea-bottom systems) in a temperate estuary to quantify standing biomass, epiphytic pest dynamics, and grazer assemblages over 12-week cultivation cycles. G. chilensis biomass was strongly seasonal, peaking in spring under low epiphytic loads and declining markedly during summer and autumn as epiphyte cover increased. Across systems, total epiphytic load exerted a significant negative effect on the final biomass, with shallow and intertidal long-line systems showing the greatest sensitivity. Ceramialean red algae were the dominant epiphytic pests, producing episodic summer blooms that frequently equalled or exceeded host biomass, while babasa-like filamentous taxa (e.g. Callithamnion sp.) accumulated more gradually and peaked in autumn, particularly in intertidal systems. Sessile invertebrates, especially hydroids, preferentially colonized deeper and more stable habitats, exhibiting progressive late-cycle accumulation. Mobile crustacean grazers were ubiquitous but seasonally mismatched with peak epiphyte outbreaks, limiting their potential for effective biocontrol. Biweekly SGR correlations confirmed temporally structured epiphytic assembly, but with finer resolutions at temporal scales. Our results demonstrate that pest pressure in G. chilensis aquaculture is strongly structured by season, cultivation depth, and system configuration. We propose that preventive, seasonally structured cultivation strategies-emphasizing spring deployment, shortened cycles, and depth optimization-offer a practical pathway to reduce epiphytic risk and improve the sustainability of pelillo farming in southern Chile.
Brown algae (Phaeophyta) encompass key primary producers of temperate and cold coastal seas, such as kelps, the cultivation of which is rapidly expanding worldwide. Here, we show that across ten brown algal species, innate resistance against the intracellular oomycete pathogen Eurychasma dicksonii is mediated by local cell death and accompanied by cell-wide deposition of β1-3 glucans and fluorescent metabolites, the accumulation of reactive oxygen species, and the expression of programmed cell death (PCD) markers. This response also occurs in compatible strains for a fraction of the infected algal cells, which makes it a quantitative trait. It is followed by the induction of two inducible autophagy-mediated defense responses already known for the oomycete pathogen Anisolpidium ectocarpii. Overall, we unveil hypersensitive-like cell death as a conserved, core part of brown algal innate defenses, that is intertwined with a second line of inducible, autophagy-mediated defenses. These results open unprecedented avenues to elucidate the molecular mechanisms of pathogen recognition and disease resistance in brown algae.
BackgroundEndoreduplication, a modified cell cycle, involves cells duplicating DNA without undergoing mitosis. This phenomenon is frequently observed in plants, algae, and animals. Biotrophic pathogens have been demonstrated to induce endoreduplication in plants to secure more space or nutrients.MethodsIn this study, we investigated the endoreduplication process triggered by two phylogenetically distant Rhizaria organisms—Maullinia spp. (in brown algae) and Plasmodiophora brassicae (in plants)—by combining fluorescent in situ hybridization (FISH) with nuclear area measurements.ResultsWe could confirm that Plasmodiophora brassicae (Plasmodiophorida) triggers endoreduplication in infected plants. For the first time, we also demonstrated pathogen-induced endoreduplication in brown algae infected with Maullinia ectocarpii and Maullinia braseltonii (Phagomyxida). We identified molecular signatures of endoreduplication in RNA-seq datasets of P. brassicae-infected Brassica oleracea and M. ectocarpii-infected Ectocarpus siliculosus.DiscussionCell cycle switch proteins such as CCS52A1 and B in plants, CCS52 in algae, and the protein kinase WEE1 in plants were upregulated in RNA-seq datasets hinting at a potential role in the phytomyxean-induced transition from mitotic cell cycle to endocycle. By demonstrating the consistent induction of endoreduplication in hosts during phytomyxid infections, our study expands our understanding of Phytomyxea–host interaction. The induction of this cellular mechanism by phytomyxid parasites in phylogenetically distant hosts further emphasizes the importance of endoreduplication in these biotrophic interactions.
Seaweed farming worldwide has increased considerably in the last century. Latin America (LATAM) has an enormous potential to contribute within the medium/long term to global seaweed production. However, the seaweed sector is not exempted by risks (e.g. diseases and pests) overall understudied in the region, reason why biosecurity and traceability measurements may be needed to some extent. In this study, policies concerning biosecurity in seaweed aquaculture in Argentina, Brazil, Chile, Colombia, Mexico and Peru were analyzed and classified for different categories. The results suggest that most of LATAM policies tend to focus on prevention measures, especially in ecological biosecurity problems, which are included mostly in general aquaculture legislations. Contrarily, economic and environmental risks are to a lesser extent covered. Furthermore, cryptic ecological aspects associated with farming such as introduction of host for diseases or genetic pollution are often overlooked, and therefore poorly managed. Within LATAM countries, Chile has the highest specificity in seaweed-exclusive legislation, likely associated to recent problems with pests and introduction of exotic species. Overall, there is a lack of information related to biosecurity risks of seaweed aquaculture in LATAM, similar to what had happened to other globally relevant producers in the southeastern Pacific that have experienced serious biosecurity problems in the recent years. Seaweed aquaculture is relatively incipient in LATAM region, but its sustainability as well as the associated food security systems may be at risk, unless new policies make compatible seaweed production and biosecurity practices.
Oomycetes are ubiquitous heterotrophs of considerable economic and ecological importance. Lately their diversity in marine environments has been shown to be greatly underappreciated and many lineages of intracellular holocarpic parasites, infecting micro- and macro-algae, remain to be fully described taxonomically. Among them, pathogens of marine red algae have been studied extensively as they infect important seaweed crops. Throughout the 20th century, most intracellular, holocarpic biotrophic oomycetes that infect red algae have been assigned to the genus Olpidiopsis Cornu. However, 18S rRNA sequencing of Olpidiopsis saprolegniae, the species considered the generitype for Olpidiopsis, suggests that this genus is not closely related to the marine pathogens and that the latter requires a nomenclatural update. Here, we compile and reanalyze all recently published 18S rRNA sequence data for marine holocarpic oomycetes, with a particular focus on holocarpic pathogens of red algae. Their taxonomy has been revised twice over the past four years, with suggestions to transfer them first into the genus Pontisma and then Sirolpidium, and into a monogeneric order, Pontismatales. We show however, that previously published topologies and the proposed taxa Pontisma, Sirolpidium, and Pontismatales are unsupported. We highlight that name changes that are unfounded and premature create confusion in interested parties, especially concerning pathogens of marine red algae that infect important seaweed crops. We thus propose that the names of these holocarpic biotrophic parasites of red algae are retained temporarily, until a supported topology is produced with more genetic markers to enable the circumscription of species and higher-level taxa.
Seaweeds are important components of coastal benthic ecosystems along the Western Antarctic Peninsula (WAP), providing refuge, food, and habitat for numerous associated species. Despite their crucial role, the WAP is among the regions most affected by global climate change, potentially impacting the ecology and physiology of seaweeds. Elevated atmospheric CO2 concentrations have led to increased dissolved inorganic carbon (Ci) with consequent declines in oceanic pH and alterations in seawater carbonate chemistry, known as Ocean Acidification (OA). Seaweeds possess diverse strategies for Ci uptake, including CO2 concentrating mechanisms (CCMs), which may distinctly respond to changes in Ci concentrations. Conversely, some seaweeds do not operate CCMs (non-CCM species) and rely solely on CO2. Nevertheless, our understanding of the status and functionality of Ci uptake strategies in Antarctic seaweeds remains limited. Here, we investigated the Ci uptake strategies of seaweeds along a depth gradient in the WAP. Carbon isotope signatures (δ13C) and pH drift assays were used as indicators of the presence or absence of CCMs. Our results reveal variability in CCM occurrence among algal phyla and depths ranging from 0 to 20 m. However, this response was species specific. Among red seaweeds, the majority relied solely on CO2 as an exogenous Ci source, with a high percentage of non-CCM species. Green seaweeds exhibited depth-dependent variations in CCM status, with the proportion of non-CCM species increasing at greater depths. Conversely, brown seaweeds exhibited a higher prevalence of CCM species, even in deep waters, indicating the use of CO2 and HCO3−. Our results are similar to those observed in temperate and tropical regions, indicating that the potential impacts of OA on Antarctic seaweeds will be species specific. Additionally, OA may potentially increase the abundance of non-CCM species relative to those with CCMs.
The Bangiales are one of the most common seaweeds in sub-Antarctic and Southeastern Pacific upper intertidal habitats. Here we report records of an 'olpidioid' marine obligate parasite infecting Bangiales between 39 degrees 20 '-41 degrees 44 ' S in the Southeastern Pacific for the first time. The disease resembles the 'Olpidiopsis blight disease' reported for farmed Bangiales in Japan and Korea and wild Pyropia from Scotland morphologically and developmentally. The Chilean isolate infects commercial Chilean laver or 'luche' (Porphyra sensu lato) and Bangia sensu lato from wild populations in the Southeastern Pacific. Phylogenetic markers (cox2, 18S) identify it as Olpidiopsis porphyrae. We relate the occurrence of this pathogen to both 'luche' fisheries in Chile and the potential consequences for its emergent aquaculture in the Southeastern Pacific.
Gracilaria chilensis (a.k.a. pelillo) is the most produced seaweed in Chile and Latin America, yet its cultivation has historically faced lots of pest-associated constrains that threat its profitability and sustainability. Pests show temporal cycles of recruitment, growth and death/senescence, variation normally linked with sharp changes in environmental factors occurring in estuarine areas whereby Gracilaria is cultivated. Here we report the appearance of a bladed Bangiales species epiphytic on long-line farmed Gracilaria and identified as Porphyra. This species recruits to cover up to 50–72
To date, the biodiversity of disease-causing agents in algae has been poorly investigated. This information however is particularly relevant, as outbreaks are repeatedly reported in mariculture facilities or commercial wild stocks, with no available baselines to compare with. Algal pathogens identified in Latin America are few; information is scattered and mostly unknown for regional aquacultural actors such as farmers, seaweed gatherers, conservation biologists and policymakers. In this work, we reviewed all the pathogens described for algae in Latin America, including their taxonomy, macro and microscopic symptoms, aetiology, habitat and reported distribution in this region. Furthermore, we included new records obtained in 2020-2022 in the Southeastern Pacific, and the results of a screen for viruses on kelp gametophytes from a regional germplasm including south Pacific and Atlantic strains. Only nine countries have described algal pathogens so far. The Southeast Pacific (Chilean coast) concentrates the largest number of records and correspond to endophytic algae of different taxa (34 %), viruses (21 %) and protistan pseudofungi (20 %). In our 2020-2022 sampling campaigns, 33 new records were reported for Latin America, which constitutes 15 % of the total records for the region. Overall, unbalanced track records were detected at geographical (e.g. country), temporal (year), diagnosis type and outbreak level, possibly due to scattered and unsystematic sampling efforts. Our results show that pathogens remain cryptic threats for seaweed-related human activities. We anticipate that as the sampling effort increases, algal pathogen records will also increase in number and importance, in proportions comparable to other ecologically and commercially relevant aquatic resources.
Macroalgae are vital reservoirs for essential epibiotic microorganisms. Among these are growth-promoting bacteria that support the growth and healthy development of their host macroalgae, and these macroalgae can be utilized in agriculture as biostimulants, offering an alternative to traditional agrochemicals. However, to date, no comparative studies have been conducted on the functional profile and bacterial diversity associated with coastal macroalgae of Peru. In this study, we employed amplicon sequencing of the V3-V4 region of 16S rRNA gene in twelve host macroalgae collected from two rocky shores in central Peru to compare their bacterial communities. The results revealed high bacterial diversity across both sites, but differences in microbial composition were noted. The phyla Bacteroidota and Pseudomonadota were predominant. The functional prediction highlighted 44 significant metabolic pathways associated with the bacterial microbiota when comparing host macroalgae. These active pathways are related to metabolism and genetic and cellular information processing. No direct association was detected between the macroalgal genera and the associated microbiota, suggesting that the bacterial community is largely influenced by their genetic functions than the taxonomic composition of their hosts. Furthermore, some species of Chlorophyta and Rhodophyta were observed to host growth-promoting bacteria, such as Maribacter sp. and Sulfitobacter sp.
Summary Phytomyxea are intracellular biotrophic parasites infecting plants and stramenopiles, including the agriculturally impactful Plasmodiophora brassicae and the brown seaweed pathogen Maullinia ectocarpii . They belong to the clade Rhizaria, where phagotrophy is the main mode of nutrition. Phagocytosis is a complex trait of eukaryotes, well documented for free‐living unicellular eukaryotes and specific cellular types of animals. Data on phagocytosis in intracellular, biotrophic parasites are scant. Phagocytosis, where parts of the host cell are consumed at once, is seemingly at odds with intracellular biotrophy. Here we provide evidence that phagotrophy is part of the nutritional strategy of Phytomyxea, using morphological and genetic data (including a novel transcriptome of M. ectocarpii ). We document intracellular phagocytosis in P. brassicae and M. ectocarpii by transmission electron microscopy and fluorescent in situ hybridization. Our investigations confirm molecular signatures of phagocytosis in Phytomyxea and hint at a small specialized subset of genes used for intracellular phagocytosis. Microscopic evidence confirms the existence of intracellular phagocytosis, which in Phytomyxea targets primarily host organelles. Phagocytosis seems to coexist with the manipulation of host physiology typical of biotrophic interactions. Our findings resolve long debated questions on the feeding behaviour of Phytomyxea, suggesting an unrecognized role for phagocytosis in biotrophic interactions.
Viruses, bacteria, and eukaryotic symbionts interact with algae in a variety of ways to cause disease complexes, often shaping marine and freshwater ecosystems. The advent of phyconomy (a.k.a. seaweed agronomy) represents a need for a greater understanding of algal disease interactions, where underestimated cryptic diversity and lack of phycopathological basis are prospective constraints for algal domestication. Here, we highlight the limited yet increasing knowledge of algal pathogen biodiversity and the ecological interaction with their algal hosts. Finally, we discuss how ecology and cultivation experience contribute to and reinforce aquaculture practice, with the potential to reshape biosecurity policies of seaweed cultivation worldwide.
ABSTRACT Endoreduplication is a modified cell cycle in which cells duplicate their DNA without subsequent mitosis. This process is common in plants and can also be found in other organisms like algae and animals. Biotrophic plant pathogens have been shown to induce endoreduplication in their host to gain space and/or nutrients. Phytomyxea (divided into the Plasmodiophorida, the Phagomyxida, and the Marinomyxa clade) are obligate biotrophic parasites of plants, diatoms, brown algae, and oomycetes. Here, we tested if phytomyxids induce local endoreduplication in two distant hosts (plants and brown algae). By combining fluorescent in situ hybridisation (FISH) coupled with nuclear area measurements and flow cytometry, we confirmed that endoreduplication is induced by Plasmodiophora brassicae (Plasmodiophorida) in infected plants and demonstrate this process in combination with Maullinia ectocarpii and Maullinia braseltonii (Phagomyxida) in brown algae. We identified molecular signatures of endoreduplication in RNA-seq datasets of P. brassicae -infected Brassica oleraceae and M. ectocarpii -infected Ectocarpus siliculosus . Cell cycle switch proteins (CCS52A1 and B in plants and CCS52 in algae) as well as the protein kinase WEE1 (in plants) were identified as genes potentially important for the phytomyxean-induced switch from the mitotic cell cycle to the endocycle. Their expression pattern changed in infected plants and brown algae accordingly. In this study we expand the knowledge on Phytomyxea-host interactions by showing that induced endoreduplication in the host is a conserved feature in phytomyxid infections. The induction of this cellular mechanism by phytomyxid parasites in phylogenetically distant hosts further points at a fundamental importance of endoreduplication in these biotrophic interactions.
SUMMARYChile is one of the top carrageenan producers worldwide, and Sarcopeltis (ex Gigartina) skottsbergii one of the topmost exploited carrageenophytes from the wild in the world. Total yield, gel strength and viscosity from two contrasting environments Calbuco and Ancud (Inner and Outer Sea, Chile) were estimated monthly in approximately 2 years for this species. While carrageenan yields did not show differences between localities, gametophytes in spring–summer had 15% higher, compared to tetrasporophytes. Sizes (frond surface) normally did not affect carrageenan yields. Gametophytes showed clear differences in gel strength between seasons, but not between localities, with maximum peaks during winter–spring months in Calbuco and autumn‐winter months in Ancud. Seasonal variations in viscosity were also significant. While gametophyte viscosity did not exceed 120 cPs, tetrasporophytes reached 1400 cPs in Calbuco and 1000 cPs in Ancud. More remarkably, a positive correlation between viscosity and gel strength was found in S. skottsbergii gametophytes, which is significantly different between both localities. These results suggest that selective harvesting in spring–summer should be preferred to optimize cost–benefit of harvesting activities and subsequent carrageenan productivity.
Worldwide, novel species of pathogens are frequently reported in cultivated and wild macroalgae. Alongside the rapid growth of the seaweed industry, diseases and pests have become an area of significant concern for cultivation and conservation of wild stocks alike: yield and quality of a crop might be greatly affected and sometimes, the losses due to diseases and pests are such that they jeopardize the economic viability of cultivation. Disease management methods and biosecurity are still in their infancy, especially as disease-causing organisms are most often poorly known, with limited options for robust and rapid diagnostics. Here, we describe a community-based, multilingual initiative that aims to foster the description of disease-causing organisms relevant to the seaweed industry worldwide and to underpin the conservation of wild seaweed genetic resources.
SummaryPhagocytosis is a complex multi-gene trait of eukaryotes and allegedly one of the very defining features of this group. Although well documented for free-living unicellular eukaryotes and in specific cellular types of animals, data on phagocytosis in intracellular biotrophic parasites are scant. Indeed, the definition of intracellular biotrophy as complete reliance of a parasite on a living host, with which it constantly negotiates for the exchange of nutrients, is at odd with the consumption of particulate matter suggested by phagocytosis. Phytomyxea are intracellular biotrophic parasites infecting a broad group of hosts, ranging from plants to stramenopiles. They belong to the clade Rhizaria, where phagotrophy (i.e., phagocytosis as main mode to acquire nutrients) is the main mode of nutrition. The exact mode of nutrition of the biotrophic phytomyxea, including the agriculturally impactful phytomyxid Plasmodiophora brassicae, is still unresolved; despite investigations and the availability of molecular data. For other Phytomyxea, observations are patchy and molecular data altogether lacking. Here, using available genomic and transcriptomic data for Phytomyxea and the de novo sequenced transcriptome of the brown algae parasite Maullinia ectocarpii, we investigate the likelihood that the genetic machinery underpinning phagotrophy is conserved within the clade. We further document intracellular phagocytosis in P. brassicae and M. ectocarpii by transmission electron microscopy and fluorescent in situ hybridization. Our investigations confirm that molecular signatures underpinning phagocytosis exist in Phytomyxea and hint at a smaller subset of genes used for intracellular phagocytosis, which is similar between the two parasites. Microscopic evidence confirms the existence of intracellular phagocytosis, which seems to coexist with the manipulation of host physiology typical of biotrophic interactions. In both phytomyxid parasites investigated intracellular phagocytosis has adapted to the intracellular environment and seemingly targets specific organelles. Our findings shed light on the feeding behaviour of Phytomyxea, providing new molecular data for the class; and suggest a paramount and previously unrecognised role for phagocytosis in biotrophic interactions between host and parasite.