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Introduction
Cyanobacteria, also known as blue-green algae, are a group of photosynthetic bacteria that play an important role in marine environments, as a source of food, oxygen production, nitrogen fixation, antibiotics production, and other bioproducts that are used by other community members (Hoffman, 1999). They are part of complex bacterial communities as biofilms (Zhong et al., 2024) and have been used as model organisms to study interactions with viruses in marine environments (Carlson et al., 2022). The picocyanobacteria Synechococcus and Prochlorococcus are the most abundant phototrophs in the global oceans, and account for a substantial fraction of marine primary production (Arias-Orozco et al., 2024; Flombaum et al., 2013).
There is a wide morphological, genetic, and functional diversity of marine cyanobacteria that is still poorly explored. They can be classified based on their morphological characteristics, including cell length and cell width of axenic culture. However, morphology does not provide sufficient taxonomic resolution and cyanobacteria with similar or identical morphology may have significantly different physiology (Nübel et al., 1997). Culturing strains is limited to replicating environmental conditions in the laboratory. Genetics and high-throughput sequencing techniques have allowed for more detailed identification of their abundance and taxonomy in marine environments. Currently, there are 431 genera and 1 653 species valid under ICN and ICNP according to the CyanoDB database (http://www.cyanodb.cz/) (Hauer & Komárek, 2022).
Understanding the diversity of marine cyanobacteria is crucial for studying key ecological processes like upwelling and cyanotoxin production, which can have significant economic and health implications (Hallegraeff, 2010). Cyanobacteria have been successful in colonizing harsh environmental conditions such as salty environments and high radiation, using halophily and halotolerance as survival strategies. These characteristics, along with their role in oxygen production and the food chain, their functions in rhodolith beds or corals, and their symbiotic relationships with invertebrates such as sponges and ascidians, are interesting to study from both ecological and evolutionary perspectives (Cavalcanti et al., 2014; Donia et al., 2011; Mutalipassi et al., 2021).
In Central America, marine cyanobacteria have been poorly explored. Most studies of this group in Costa Rica focus on field observations, with few specimens in herbaria. Therefore, the objectives of this work were to compile cyanobacterial diversity in Costa Rican marine environments based on scientific publications and collections in herbaria as a baseline for future research.
Materials and methods
Scientific articles and books from 1936 (the first record) to the present were reviewed, and a list of the genera and in some cases species of cyanobacteria reported from the Costa Rican Pacific and Caribbean Sea was compiled by location. In November 2023, the Dr. Luis A. Fournier Origgi Herbarium (USJ) at Escuela de Biología of the Universidad de Costa Rica was visited to review the cyanobacteria specimens. There are no other herbarium collections of marine cyanobacteria in the country.
The list of cyanobacteria was arranged according to the subdivisions proposed by Rippka et al. (1979), which are based on differences in morphological structure and development, allowing the recognition of five major sections among cyanobacteria (I, II, III, IV, and V). The taxonomic classification at the genus level was based on the system proposed in AlgaeBase (Guiry & Guiry, 2024). For each report, the taxonomic classification at the order, family, and genus levels, the collection site, and the references are provided.
The search for DNA sequences of marine cyanobacteria from Costa Rica was conducted in 2023 and 2024 using the NCBI (The National Center for Biotechnology Information), and ENA (European Nucleotide Archive) databases (Burgin et al., 2023), as well as scientific articles. We focused on nucleotide sequences, genomes, MAGs (Metagenome Assembled Genomes), and bioprojects.
Results
We found 50 records of cyanobacteria in the references and in the herbarium, 10 belong to Sections I and II, 26 in Section III, nine to Section IV and five under unclassified category. A total of 20 species are reported from the Pacific and 33 from the Caribbean with three species/genus in common, Symploca hydnoides, Schizothrix calcicola and Spirulina spp. Trichodesmium erythraeum, Symploca spp. and Lyngbya spp. have the highest number of records, with Symploca having the most herbarium accessions.
Unicellular cyanobacteria (Section I and Section II): We found ten species in these sections. Among the unicellular cyanobacteria reported in the literature are the genera Merismopedia, Anacystis, Synechocystis, Synechococcus, and Prochlorococcus (Table 1). Belonging to Section II, we find Chamaecalyx in the Orden Pleurocapsales. Chrococcales has the largest number of reported species, but the genera Synechococcus and Prochlorocococcus have been reported from a greater number of sites. The reports of these groups were based on culture-independent techniques, while others were based on optical microscopy.
Table 1 Marine cyanobacteria that belong to the orders Chroococcales, Synechococcales and Pleurocapsales (Sections I and II) and its geographic distribution in Costa Rica.
| Order | Family | Genus/species | Biogeographic distribution | References |
| Chroococcales | Chamaesiphonaceae | Stichosiphon sansibaricus (Hieronymus) F. E.Drouet & W.A.Daily, 1956 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Chroococcaceae | Chroococcus sp. Nägeli, 1849 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) | |
| Cyanothrichaceae | Johannesbaptistia pellucida (Dickie) W.R.Taylor & Drouet, 1938 | Caribbean: Isla Uvita | Muñoz-Simon (2012), Muñoz-Simon et al. (2020) | |
| Microcystaceae | Anacystis sp. Meneghini, 1837 | Pacific: Golfo de Papagayo | Loza-Álvarez et al. (2018) | |
| Merismopedia glauca (Ehrenberg) Kützing, 1845 | Pacific: Bahía Culebra | Cortés et al. (2012), Drouet, (1936) | ||
| Merismopedia elegans A.Braun ex Kützing 1849 | Pacific: Gulf of Nicoya | Calvo Vargas et al. (2014) | ||
| Synechocystis sp. Sauvageau, 1892 | Caribbean: Isla Uvita | Muñoz-Simon et al. (2020) | ||
| Pleurocapsales | Hyellaceae | Chamaecalyx leibleiniae (Reinsch) Komárek & Anagnostidis, 1986 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Synechococcales | Synechococcaceae | Synechococcus sp. Nägeli, 1849 | Pacific: Costa Rica Thermal Dome | Ahlgren et al. (2014), Cox et al. (2014), Gutiérrez-Rodríguez et al., (2014), Saito et al. (2005) |
| Prochlorococcaceae | Prochlorococcus sp. Chisholm, Frankel, Goericke, Olson, Palenik, Waterbury, West-Johnsrud & Zettler ex Komárek et al., 2020 | Pacific: Isla del Coco National Park; Open ocean, 30 miles from Isla del Coco; and Costa Rica Thermal Dome | Ahlgren et al. (2014), Cortés (2012), Cox et al. (2014), Gutiérrez-Rodríguez et al. (2014), Williamson et al. (2008) |
The taxonomic classification is based on Algae Base.
Filamentous cyanobacteria without heterocysts (Section III): This is the group of cyanobacteria with the most reports, there are 22 species in the Caribbean and seven species in the Pacific (Table 2). This reflects the higher sampling effort along the Caribbean coast. Oscillatoriales is the most reported order, followed by Coleofasciculae. These groups are characterized by being filamentous and are often the main phototrophic component of the biofilms. Interestingly, the genus Spirulina, which is widely used in the food industry, was reported from both coasts.
Table 2 Marine cyanobacteria belonging to the orders Oscillatoriales, Leptolyngbyales, Pseudanabaenales, Coleofasciculales, Geitlerinematales, Spirulinales and Gomontiellales (Section III) and its geographic distribution in Costa Rica.
| Order | Family | Genus/species | Biogeographic distribution | References |
| Coleofasciculales | Coleofasciculaceae | Coleofasciculus chthonoplastes (Gomont) M.Siegesmund, J.R.Johansen & T.Friedl 2008 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Symploca sp. Kützing ex Gomont, 1892 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) | ||
| Symploca hydnoides Kützing ex Gomont, 1892 | Caribbean: Vicinity of Puerto Limón, Portete, Parque Nacional Cahuita Pacific: Isla Bolaños, Bahía Salinas, Playa Sámara, Cangrejal, Península de Nicoya, Isla del Caño | Dawson (1962); USJ-73046, USJ-73108, USJ-73152, USJ-73305, USJ-73341, USJ-73498, USJ-73528, USJ-73537, USJ-73570, USJ-73686 | ||
| Symploca hydnoides var. fasciculata Gomont, 1892 | Caribbean: Portete | Dawson (1962) | ||
| Symploca thermalis Gomont, 1892 | Pacific: Isla del Caño | USJ-73837 | ||
| Geitlerinematales | Geitlerinemataceae | Geitlerinema cf. exile (Skuja) Anagnostidis, 1989 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Gomontiellales | Gomontiellaceae | Borzia sp. Cohn ex Gomont, 1892 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Leptolyngbyales | Leptolyngbyaceae | Leptolyngbya sp. Anagnostidis & Komárek, 1988, nom. et typ. cons. | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Trichocoleusaceae | Schizothrix sp. Kützing ex Gomont, 1892 | Caribbean: Cahuita National Park | USJ-73851 | |
| Schizothrix calcicola var. symplociformis Hansgirg ex Elenkin, 1949 | Caribbean: Vicinity of Puerto Limón Pacific: Playa Manuel Antonio (reported as Playa Manuel Garcia) | Dawson (1962) | ||
| Oscillatoriales | Microcoleaceae | Blennothrix cantharidosma (Gomont) Anagnostidis & Komárek, 1988 as Hydrocoleum cantharidosmum | Pacific: Bahía Culebra | Cortés et al., 2012; Drouet, 1936 |
| Leibleinia gracilis (Rabenhorst ex Gomont) Anagnostidis & Komárek, 1988 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) | ||
| Lyngbya sp. C.Agardh ex Gomont, 1892, nom. et typ. cons. | Caribbean: Isla Uvita | Muñoz-Simon (2012) | ||
| Lyngbya majuscula Harvey ex Gomont, 1892 | Caribbean: Vicinity of Puerto Limón | Dawson (1962) | ||
| Lyngbya sordida f. bostrychicola Gomont, 1892 | Caribbean: Portete, Vicinity of Puerto Limón | Dawson (1962) | ||
| Lyngbya subconfervoides O.Borge, 1918 | Caribbean: Cahuita National Park | Bernecker & Wehrtmann, (2009) | ||
| Microcoleus chthonoplastes Thuret ex Gomont, 1892 | Caribbean: Puerto Vargas | Dawson (1962) | ||
| Trichodesmium erythraeum Ehrenberg ex Gomont, 1892 | Pacific: Bahía Culebra, Gulf of Nicoya, Caldera | Calvo Vargas et al. (2014), Calvo Vargas et al. (2016), Vargas-Montero (2004), Vargas-Montero & Freer (2004) | ||
| Oscillatoriaceae | Oscillatoria sp. Vaucher ex Gomont, 1892 | Caribbean: Isla Uvita | Muñoz-Simon (2012), Muñoz-Simon et al. (2020) | |
| Oscillatoria corallinae Gomont, 1890 | Caribbean: Vicinity of Puerto Limón | Dawson (1962) | ||
| Phormidium sp. Kützing ex Gomont, 1892 | Caribbean: Isla Uvita | Muñoz-Simon (2012), Muñoz-Simon et al. (2020) | ||
| Phormidium crosbyanum Tilden, 1909 | Caribbean: Undefined site | Dawson (1962) | ||
| Phormidium monile Setchell & Gardner, 1930 as Lyngbya gracilis | Pacific: Bahía Culebra | Taylor (1945) | ||
| Pseudanabaenales | Pseudanabaenaceae | Pseudanabaena sp. Lauterborn, 1915 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) |
| Spirulinales | Spirulinaceae | Spirulina sp. Turpin ex Gomont, 1892 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo Pacific: Mangrove sediments, Golfo Dulce | Medeanic et al. (2008); Muñoz-Simon (2012) |
| Spirulina subsalsa Oersted ex Gomont, 1892 | Caribbean: Parque Nacional Cahuita | Hargraves & Víquez (1981) |
The taxonomic classification is based on Algae Base. Codes correspond to USJ-Herbaria Collection number, Universidad de Costa Rica.
Filamentous cyanobacteria with heterocysts and true branching (Section IV): The genera Isactis, Calothrix, Rivularia, Anabaena, Bachytrichia, and Nodularia were found within the Order Nostocales, each belonging to different families (Table 3). All these genera possess heterocysts, which makes them potential nitrogen fixers. Nitrogen-fixing cyanobacteria play an important role in transforming elemental nitrogen into bioavailable nitrogen, which is of great importance for food chains.
Table 3 Marine cyanobacteria belonging to the Order Nostocales (Section IV) and its geographic distribution in Costa Rica.
| Order | Family | Genus/species | Biogeographic distribution | References |
| Nostocales | Aphanizomenonaceae | Anabaena sp. Bory ex Bornet & Flahault, 1886, nom. cons. | Pacific: Mangrove sediments, Golfo Dulce | Medeanic et al. (2008) |
| Nodulariaceae | Nodularia harveyana Thuret ex Bornet & Flahault, 1886 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) | |
| Nostocaceae | Nostoc commune (Vaucher ex Bornet et Flahault 1888) | Caribbean: Punta Manzanillo | USJ-28295 | |
| Rivulariaceae | Calothrix C.Agardh ex Bornet & Flahault, 1886 | Caribbean: Piuta, Isla Uvita, Puerto Vargas, Puerto Viejo, Manzanillo | Muñoz-Simon (2012) | |
| Calothrix crustacea f. simulans F.S.Collins, 1907 | Caribbean: Vicinity of Puerto Limón | Dawson (1962) | ||
| Calothrix pilosa Harvey ex Bornet & Flahault, 1886 | Caribbean: Vicinity of Puerto Limón | Dawson (1962) | ||
| Isactis plana (Harvey) Thuret ex Bornet & Flahault, 1886 | Pacific: Bahía Culebra | Taylor (1945) | ||
| Rivularia sp. C.Agardh ex Bornet & Flahault, 1886, nom. cons. | Pacific: Mangrove sediments, Golfo Dulce | Medeanic et al. (2008) | ||
| Scytonemataceae | Brachytrichia quoyi Bornet & Flahault, 1886 | Caribbean: Puerto Vargas | Dawson (1962) |
The taxonomic classification is based on Algae Base. Codes correspond to USJ-Herbaria Collection number, Universidad de Costa Rica.
Unclassified cyanobacteria: Investigations carried out in the Pacific using light microscopy or independent culture techniques reported five samples as unclassified cyanobacteria (Table 4).
Table 4 Unclassified marine cyanobacteria of Costa Rica and its geographic distribution.
| Order | Family | Genus/specie | Biogeographic distribution | References |
| unc. Cyanobacteria | unc. Cyanobacteria | unc. Cyanobacteria | Pacific: Isla del Coco National Park | Fernández (2008) |
| unc. Cyanobacteria | Pacific: Área de Conservación Guanacaste | Cortés & Joyce (2020) | ||
| unc. Cyanobacteria | Pacific: Coral reefs and submerged pinnacles around Isla del Caño Biological Reserve; coastal rocky reefs and islets along the Osa Peninsula, including Corcovado National Park | Friedlander et al. (2022) | ||
| unc. Cyanobacteria | Pacific: Golfo Dulce | Steinsdóttir et al. (2022) | ||
| unc. Cyanobacteria | Pacific: In front of Punta Copal, Isla Bolaños, Bahía Salinas, Guanacaste | USJ-73735 |
The taxonomic classification is based on Algae Base. Codes correspond to USJ-Herbaria Collection number, Universidad de Costa Rica.
We found two studies that focused on cyanobacterial genome analysis (Table 5). Zehr et al. (2007) investigated the genomic diversity of tropical oceanic nitrogen-fixing cyanobacteria in the Dome Upwellling Zone in Pacific Costa Rica, obtaining cultures and amplifying the region encoding the cytochrome C gene using Sanger sequencing. The second study by Niemann et al. (2013) examined the bacterial communities associated with the decapod Paralomis.
Table 5 DNA sequences of cyanobacteria in the NCBI and ENA databases.
| Site/Bioproject | Accesion ID | Taxonomic classification | Reference |
| Costa Rica Dome Upwelling Zone (8 m depth) | EF102542 | unclassified Cyanobacteria | Zehr et al. (2007) |
| EF102614 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| EF102613 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| EF102612 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| EF102611 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| EF102590 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| EF102573 | unclassified Cyanobacteria | Zehr et al. (2007) | |
| Stomach content of the crab Paralomis sp. | HE974904 | Uncultured Cyanobacterium sp. | Niemann et al. (2013) |
Discussion
Published reports of cyanobacteria from the Pacific and the Caribbean of Costa Rica do not have photographs, and most of these reports lack data on temperature, salinity, pH, substrate type, or other metadata, which limits our understanding of the ecology of these group. Additionally, these cyanobacteria are not associated with herbarium specimens. There are only 14 cyanobacterial samples in the herbaria collection. The improvement of herbarium records and sample conservation would support the training of future scientists. High-quality collections serve as invaluable resources for teaching taxonomy, systematics, ecology, and fostering the development of new expertise in these fields. Plus, it increases the knowledge of the marine biodiversity of the country.
Due to traditional sampling techniques, where larger micro-organisms are more likely to be studied, unicellular cyanobacteria or pycocyanobacteria are probably among the least studied. The classification of cyanobacteria is undergoing rapid change due to advances in 16S rRNA gene and genome sequencing, independent and dependent culture techniques can now be used to characterize them, as well as other groups of cyanobacteria (Chen et al., 2021; Doré et al., 2023). Taxonomic studies must be polyphasic, incorporating morphological data such as cell size and shape, presence or absence of a mucilaginous sheath, and shape of apical cells, among others (Hauer & Komarék, 2022). The integration of genomic data is essential for conclusively defining the taxonomic clades of many cyanobacterial genera. The morphological similarity between some groups, such as the Leptolyngbya clade in Section III (Brenes-Guillén et al., 2021; Komarek, 2007), could be studied in marine environments to understand the coexistence of phylogenetic closely and ecologically similar cyanobacterial species.
There are several studies that summarize the cyanobacteria found in the region. Vargas et al. (2023) carried out a review of the diversity in the Caribbean region and reported 76 genera and 119 species of cyanobacteria associated with different environments such as coral reefs, ascidians, mangroves and others. In that study, Lyngbya confervoides is the only cyanobacteria mentioned for Costa Rica (based on the report by Bernecker & Wehrtmann, 2009), unlike our research where we report 33 species for the Caribbean. Studies in Honduras and Belize indicate that new genera similar to the genera Lyngbya and Symploca may be found in marine environments (Engene et al., 2015). In Panama, studies on marine cyanobacteria have focused on the extraction of metabolites to identify novel treatments for neglected parasitic diseases such as malaria. The Panama International Cooperative Biodiversity Group (ICBG) programme has investigated secondary metabolites mainly from Leptolyngbya, Symploca, Lyngbya and Oscillatoria (Linington et al., 2007; McPhail et al., 2007; Medina et al., 2008; Simmons et al., 2006; Vining et al., 2015). Additionally, Diaz et al. (2007) found Oscillatoria spongeliae associated with marine sponges in the Caribbean Sea of Panama.
Some groups of marine cyanobacteria are symbionts of protozoa, macroalgae, seagrasses, sponges, ascidians, and other invertebrates, altering the host’s metabolism (Carpenter & Foster, 2002; Konstantinou et al., 2018; Mutalipassi et al., 2021). In addition, they possess cellular and molecular strategies that enable them to withstand nutrient limitation, temperature fluctuations, increased UV radiation, and high salinity (Li et al., 2019; Rastogi et al., 2014; Reignier et al., 2023). These characteristics suggest that these bacteria may have promising biotechnological applications. Current evidence shows the presence of marine cyanobacteria on both coasts of Costa Rica, highlighting their importance, but the morphological and genetic diversity of cyanobacteria in Costa Rican and Central Americans marine environments remains largely unknown. In order to improve our understanding of the taxonomic and functional diversity of cyanobacteria, it is essential to conduct studies focusing on morphological and genetic analysis, either using molecular markers such as 16S gene amplicons or whole genome sequencing. This will provide information on the microscopic characterization of cyanobacteria, their biogeographic distribution, temporal variations in abundance and the genetic reservoir. This publication will serve as a basis and motivation for future research.
Ethical statement: the authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. All financial sources are fully and clearly stated in the acknowledgments section. A signed document has been filed in the journal archives.
