Dinoroseobacter shibae

Last updated

Dinoroseobacter shibae
Scientific classification
Domain:
Phylum:
Class:
Order:
Family:
Genus:
Species:
D. shibae
Binomial name
Dinoroseobacter shibae
Biebl et al. 2005

Dinoroseobacter shibae is a facultative anaerobic anoxygenic photoheterotroph belonging to the family, Rhodobacteraceae. First isolated from washed cultivated dinoflagellates, they have been reported to have mutualistic as well as pathogenic symbioses with dinoflagellates.

Contents

Cell morphology and physiology

D. shibae cells are Gram-negative cocci, or occasionally ovoid rods that measure 0.3 – 0.7 μm in width and 0.3 – 1.0 μm in length. [1] They are motile and have a single polar flagellum.

When grown in the dark, colonies have a distinct pink or light red pigmentation, while under strong illumination they are beige. They contain bacteriochlorophyll a and the carotenoid pigment spheroidenone and have absorption spectrum peaks at 804 and 868 nm. The carotenoid leads to an extended absorption spectrum including 400 – 600 nm. [1] D. shibae cells use light as a supplementary energy source and don't use it to fix inorganic carbon. [2] Colonies grown on complex agar media appear deep red in color. [1]

D. shibae is a facultative anaerobe that requires 1-7% salinity and grows between 15 and 38 °C with an optima temperature of 33 °C. Its optimal pH range is 6.5 – 9.0. [1] While most of the organisms in the Roseobacter clade are obligate aerobes, D. shibae is able to grow anaerobically using electron acceptors nitrate and dimethyl sulfoxide. [3] It has a complete denitrification pathway for energy production. [3] A variety of organic substrates including acetate, succinate, fumarate, malate, lactate, citrate, glutamate, pyruvate, glucose, fructose and glycerol can support heterotrophic growth. Like others in the Roseobacter clade, ethanol, methanol and butyrate do not support growth. [1]

D. shibae can synthesize vitamins and , of which its dinoflagellate host is auxotrophic. [3]

Environment and ecology

Members of the Roseobacter clade are widely associated with marine phytoplankton such as dinoflagellates and diatoms in the water column as well as shallow sediments. They play important roles in the carbon cycle by assimilating dissolved organic matter produced by phytoplankton and also in the sulfur cycle by removing DMS from the algal osmolyte dimethylsulfoniopropionate (DMSP). [4] Their close association with eukaryotic phytoplankton is supported by phylogenomic evidence suggesting that the Roseobacter lineage diverged from other Alphaproteobacteria at the same moment as the Mesozoic radiation of phytoplankton. [4]

Traits involved in symbioses of D. shibae include flagellar synthesis and type IV secretion system under the control of N-acyl homoserine lactone intercellular signal molecules (quorum sensing). [4]

D. shibae forms symbioses with Prorocentrum minimum, a toxic red tide-forming dinoflagellate, as well as other dinoflagellates associated with toxic algal blooms. In a mutualistic association, the P. minimum provides carbon sources and some vitamins essential for growth, and while D. shibae provides vitamins and . In co-culture, this mutualism changes to pathogenicity as the bacteria induce death in the algae cells, but algicidal compounds produced by D. shibae have yet to be identified. [4] P. minimum has a global marine distribution, suggesting that its symbiont does as well. [4]

Genome

D. shibae’s genome is 4417 kbp long, which is in line with other Roseobacter clade genomes. [3] Included in this count are its large circular genome and five circular plasmids. The GC-content of D. shibae is 66%.

Based on comparative sequence analysis of the circular plasmids, they were likely acquired through conjugation and two sister plasmids contain the vir operon encoding the type IV secretion system required for the formation of sex pili. Other traits encoded on the plasmids include degradation of aromatic compounds and carbon monoxide oxidation. [3]

As opposed to ABC transporters, the D. shibae genome suggests a preference for tripartite ATP-independent periplasmic transporters (TRAP) for uptake of nutrients like C4-dicarboxylates, pyruvate, glutamate, sialic acid, ectoine and 2,3-diketogulonate. [3] D. shibae’s genome encodes for 27 complete TRAP systems.

Discovery and Isolation

D. shibae was first isolated in 2003 with two strains, both isolated from washed single cells of cultivated marine dinoflagellates (Prorocentrum lima and Alexandrium ostenfeldii). [1]

Etymology

The genus Dinoroseobacter name originates from the Greek dinos meaning whirling rotation and the first part of Dinophyceae (dinoflagellates) from which it was isolated, and Roseobacter a bacterial genus with similar traits. Shibae was named after Professor Tsuneo Shiba who discovered the marine aerobic anoxygenic phototrophic bacteria. [1]

Related Research Articles

Acantharea Class of single-celled organisms

The Acantharea (Acantharia) are a group of radiolarian protozoa, distinguished mainly by their strontium sulfate skeletons. Acantharians are heterotrophic marine microplankton that range in size from about 200 microns in diameter up to several millimeters. Some acantharians have photosynthetic endosymbionts and hence are considered mixotrophs.

Endosymbiont Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes; single-cell algae inside reef-building corals, and bacterial endosymbionts that provide essential nutrients to about 10–15% of insects.

Zooplankton Heterotrophic protistan or metazoan members of the plankton ecosystem

Zooplankton are heterotrophic plankton. Plankton are organisms drifting in oceans, seas, and bodies of fresh water. The word zooplankton is derived from the Greek zoon (ζῴον), meaning "animal", and planktos (πλαγκτός), meaning "wanderer" or "drifter". Individual zooplankton are usually microscopic, but some are larger and visible to the naked eye.

Zooxanthellae Dinoflagellates in symbiosis with coral, jellyfish and nudibranchs

Zooxanthellae is a colloquial term for single-celled dinoflagellates that are able to live in symbiosis with diverse marine invertebrates including demosponges, corals, jellyfish, and nudibranchs. Most known zooxanthellae are in the genus Symbiodinium, but some are known from the genus Amphidinium, and other taxa, as yet unidentified, may have similar endosymbiont affinities. The true Zooxanthella K.brandt is a mutualist of the radiolarian Collozoum inerme and systematically placed in Peridiniales. Another group of unicellular eukaryotes that partake in similar endosymbiotic relationships in both marine and freshwater habitats are green algae zoochlorellae.

Chromatiaceae Family of purple sulfur bacteria

The Chromatiaceae are one of the two families of purple sulfur bacteria, together with the Ectothiorhodospiraceae. They belong to the order Chromatiales of the class Gammaproteobacteria, which is composed by unicellular Gram-negative organisms. Most of the species are photolithoautotrophs and conduct an anoxygenic photosynthesis, but there are also representatives capable of growing under dark and/or microaerobic conditions as either chemolithoautotrophs or chemoorganoheterotrophs.

Methylotrophs are a diverse group of microorganisms that can use reduced one-carbon compounds, such as methanol or methane, as the carbon source for their growth; and multi-carbon compounds that contain no carbon-carbon bonds, such as dimethyl ether and dimethylamine. This group of microorganisms also includes those capable of assimilating reduced one-carbon compounds by way of carbon dioxide using the ribulose bisphosphate pathway. These organisms should not be confused with methanogens which on the contrary produce methane as a by-product from various one-carbon compounds such as carbon dioxide. Some methylotrophs can degrade the greenhouse gas methane, and in this case they are called methanotrophs. The abundance, purity, and low price of methanol compared to commonly used sugars make methylotrophs competent organisms for production of amino acids, vitamins, recombinant proteins, single-cell proteins, co-enzymes and cytochromes.

<i>Symbiodinium</i> Genus of dinoflagellates (algae)

Symbiodinium is a genus of dinoflagellates that encompasses the largest and most prevalent group of endosymbiotic dinoflagellates known. These unicellular microalgae commonly reside in the endoderm of tropical cnidarians such as corals, sea anemones, and jellyfish, where the products of their photosynthetic processing are exchanged in the host for inorganic molecules. They are also harbored by various species of demosponges, flatworms, mollusks such as the giant clams, foraminifera (soritids), and some ciliates. Generally, these dinoflagellates enter the host cell through phagocytosis, persist as intracellular symbionts, reproduce, and disperse to the environment. The exception is in most mollusks, where these symbionts are intercellular. Cnidarians that are associated with Symbiodinium occur mostly in warm oligotrophic (nutrient-poor), marine environments where they are often the dominant constituents of benthic communities. These dinoflagellates are therefore among the most abundant eukaryotic microbes found in coral reef ecosystems.

<i>Roseobacter</i> Genus of bacteria

In taxonomy, Roseobacter is a genus of the Rhodobacteraceae. The Roseobacter clade falls within the {alpha}-3 subclass of the class Alphaproteobacteria. The first strain descriptions appeared in 1991 which described members Roseobacterlitoralis and Roseobacterdenitrificans, both pink-pigmented bacteriochlorophyll a-producing strains isolated from marine algae. The role members of the Roseobacter lineage play in marine biogeochemical cycles and climate change cannot be overestimated. Roseobacters make up 25% of coastal marine bacteria and members of this lineage process a significant portion of the total carbon in the marine environment. Roseobacter clade plays an important role in global carbon and sulphur cycles. It can also degrade aromatic compounds, uptake trace metal, and form symbiotic relationship. In term of its application, Roseobacter clade produces bioactive compounds, has been used widely in aquaculture and quorum sensing.

Cyanobionts are cyanobacteria that live in symbiosis with a wide range of organisms such as terrestrial or aquatic plants; as well as, algal and fungal species. They can reside within extracellular or intracellular structures of the host. In order for a cyanobacterium to successfully form a symbiotic relationship, it must be able to exchange signals with the host, overcome defense mounted by the host, be capable of hormogonia formation, chemotaxis, heterocyst formation, as well as possess adequate resilience to reside in host tissue which may present extreme conditions, such as low oxygen levels, and/or acidic mucilage. The most well-known plant-associated cyanobionts belong to the genus Nostoc. With the ability to differentiate into several cell types that have various functions, members of the genus Nostoc have the morphological plasticity, flexibility and adaptability to adjust to a wide range of environmental conditions, contributing to its high capacity to form symbiotic relationships with other organisms. Several cyanobionts involved with fungi and marine organisms also belong to the genera Richelia, Calothrix, Synechocystis, Aphanocapsa and Anabaena, as well as the species Oscillatoria spongeliae. Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations.

<i>Chrysochromulina</i> Genus of single-celled organisms

Chrysochromulina is a genus of haptophytes. This phytoplankton is distributed globally in brackish and marine waters across approximately 60 known species. All Chrysochromulina species are phototrophic, however some have been shown to be mixotrophic, including exhibiting phagotrophy under certain environmental conditions. The cells are small, characterized by having scales, and typically observed using electron microscopy. Some species, under certain environmental conditions have been shown to produce toxic compounds that are harmful to larger marine life including fish.

<i>Ornithocercus</i> Genus of single-celled organisms

Ornithocercus is a genus of planktonic dinoflagellate that is known for its complex morphology that features considerable lists growing from its thecal plates, giving an attractive appearance. Discovered in 1883, this genus has a small number of species currently categorized but is widespread in tropical and sub-tropical oceans. The genus is marked by exosymbiotic bacteria gardens under its lists, the inter-organismal dynamics of which are a current field of research. As they reside only in warm water, the genus has been used as a proxy for climate change and has potential to be an indicator species for environmental change if found in novel environments.

Aerobic anoxygenic phototrophic bacteria (AAPBs) are alphaproteobacteria and gammaproteobacteria that are obligate aerobes that capture energy from light by anoxygenic photosynthesis. Anoxygenic photosynthesis is the phototrophic process where light energy is captured and stored as ATP. The production of oxygen is non-existent and, therefore, water is not used as an electron donor. They are widely distributed marine plankton that may constitute over 10% of the open ocean microbial community. They can be particularly abundant in oligotrophic conditions where they were found to be 24% of the community. Aerobic anoxygenic phototrophic bacteria are photoheterotrophic (phototroph)microbes that exist in a variety of aquatic environments. Photoheterotrophs, are heterotrophic organisms that use light to produce energy, but are unable to utilize carbon dioxide as their primary carbon source. Most are obligately aerobic, meaning they require oxygen to grow. One remarkable aspect of these novel bacteria is that they, unlike other similar bacteria, are unable to utilize BChl (bacteriochlorophyll) for anaerobic growth. The only photosynthetic pigment that exists in AAPB is BChl a. Anaerobic phototrophic bacteria, on the contrary, can contain numerous species of photosynthetic pigments like bacteriochlorophyll a, b, c, d, e, f, etc. There is still a large void in the areas regarding the abundance and genetic diversity of the AAPB, as well as the environmental variables that regulate these properties.

Marine microorganisms Any life form too small for the naked human eye to see that lives in a marine environment

Marine microorganisms are defined by their habitat as microorganisms living in a marine environment, that is, in the saltwater of a sea or ocean or the brackish water of a coastal estuary. A microorganism is any microscopic living organism or virus, that is too small to see with the unaided human eye without magnification. Microorganisms are very diverse. They can be single-celled or multicellular and include bacteria, archaea, viruses and most protozoa, as well as some fungi, algae, and animals, such as rotifers and copepods. Many macroscopic animals and plants have microscopic juvenile stages. Some microbiologists also classify biologically active entities such as viruses and viroids as microorganisms, but others consider these as non-living.

Rhodoferax is a genus of Betaproteobacteria belonging to the purple nonsulfur bacteriarophic. Originally, Rhodoferax species were included in the genus Rhodocyclus as the Rhodocyclus gelatinous-like group. The genus Rhodoferax was first proposed in 1991 to accommodate the taxonomic and phylogenetic discrepancies arising from its inclusion in the genus Rhodocyclus. Rhodoferax currently comprises four described species: R. fermentans, R. antarcticus, R. ferrireducens, and R. saidenbachensis. R. ferrireducens, lacks the typical phototrophic character common to two other Rhodoferax species. This difference has led researchers to propose the creation of a new genus, Albidoferax, to accommodate this divergent species. The genus name was later corrected to Albidiferax. Based on geno- and phenotypical characteristics, A. ferrireducens was reclassified in the genus Rhodoferax in 2014. R. saidenbachensis, a second non-phototrophic species of the genus Rhodoferax was described by Kaden et al. in 2014.

Phycosphere Microscale mucus region that is rich in organic matter surrounding a phytoplankton cel

The phycosphere is a microscale mucus region that is rich in organic matter surrounding a phytoplankton cell. This area is high in nutrients due to extracellular waste from the phytoplankton cell and it has been suggested that bacteria inhabit this area to feed on these nutrients. This high nutrient environment creates a microbiome and a diverse food web for microbes such as bacteria and protists. It has also been suggested that the bacterial assemblages within the phycosphere are species-specific and can vary depending on different environmental factors.

Nassellaria Order of single-celled organisms

Nassellaria is an order of Rhizaria belonging to the class Radiolaria. The organisms of this order are characterized by a skeleton cross link with a cone or ring.

"Candidatus Karelsulcia muelleri" is an aerobic, gram-negative, bacillus bacterium that is a part of the phylum Bacteroidetes. "Ca. K. muelleri" is an obligate and mutualistic symbiotic microbe commonly found occupying specialized cell compartments of sap-feeding insects called bacteriocytes. A majority of the research done on "Ca. K. muelleri" has detailed its relationship with the host Homalodisca vitripennis. Other studies have documented the nature of its residency in other insects like the maize leafhopper (Cicadulina) or the spittlebug (Cercopoidea). "Ca. K. muelleri" is noted for its exceptionally minimal genome and it is currently identified as having the smallest known sequenced Bacteroidetes genome at only 245 kilobases.

Congregibacter litoralis KT71 is a gram-negative Gammaproteobacteria part of the NOR5/OM60 Clade discovered in seawater from Heligoland, an island in the North Sea by H. Eilers from the Max Planck Institute for Microbiology. C. litoralis KT71 is described as a pleomorphic bacterium and has a size of 2 x 0.5 μm. When grown in culture, C. litoralis KT71 has a generation time of 4.5 hours and prefers to grow on complex substrates where the sole carbon source is undefined, though it can utilize some sole carbon sources because they are most likely used by the organism for its central metabolism.

Rhodomicrobium vannielii is a Gram-negative, purple non-sulfur, motile, thermophilic photoheterotroph bacterium. Phototrophic bacteria are ubiquitous and have been reportedly found in many marine and terrestrial ecosystems. Additionally, they can use light as an energy source and carbon dioxide as a carbon source. Considering this, R. vannielii is thought to have potential application in anaerobic treatment and bioremediation under high temperature conditions as the bacteria was isolated from water samples from a hot spring in Gadek, Malacca, Malaysia using glutamate-malate medium (GMM) and Pfennig's M2 medium. R. vannielii produces acyclic and aliphatic cyclic carotenoids like anhydrorhodovibrin, rhodovibrin, spirilloxanthin and rhodopin.

Mixotrophic dinoflagellate Plankton

Dinoflagellates are eukaryotic plankton, existing in marine and freshwater environments. Previously, dinoflagellates had been grouped into two categories, phagotrophs and phototrophs. Mixotrophs, however include a combination of phagotrophy and phototrophy. Mixotrophic dinoflagellates are a sub-type of planktonic dinoflagellates and are part of the phylum Dinoflagellata. They are flagellated eukaryotes that combine photoautotrophy when light is available, and heterotrophy via phagocytosis. Dinoflagellates are one of the most diverse and numerous species of phytoplankton, second to diatoms.

References

  1. 1 2 3 4 5 6 7 Biebl, H.; Allgaier, M.; Tindall, B. J.; Koblizek, M.; Lünsdorf, H.; Pukall, R.; Wagner-Döbler, I. (2005). "Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates". International Journal of Systematic and Evolutionary Microbiology. 55 (3): 1089–1096. doi: 10.1099/ijs.0.63511-0 . PMID   15879238.
  2. Soora, M.; Cypionka, H. (2013). "Light Enhances Survival of Dinoroseobacter shibae during Long-Term Starvation". PLOS ONE. 8 (12): e83960. Bibcode:2013PLoSO...883960S. doi: 10.1371/journal.pone.0083960 . PMC   3875502 . PMID   24386315.
  3. 1 2 3 4 5 6 Wagner-Dobler, I.; Ballhausen, B.; Berger, M.; Brinkhoff, T.; Buchholz, I.; Bunk, B.; Simon, M. (2009). "The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea". ISME J. 4 (1): 61–77. doi: 10.1038/ismej.2009.94 . PMID   19741735.
  4. 1 2 3 4 5 Wang H, Tomasch J, Jarek M, Wagner-Dobler I: A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates. Frontiers of Microbiology 2014, 5:311.