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Draft:Macroalgae Microbiome

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  • Comment: I'm getting a pretty strong feeling that this may have been written by AI. Pbritti (talk) 05:14, 6 April 2024 (UTC)
Brown algae, a common macroalgae home to many different types of microbiomes.

A macroalga microbiome describes the dynamic communities of microorganisms living in symbiosis with a macroalga, which are often regarded together as a unit called a holobiont.[1]. Macroalgae is a broad term for thousands of species of multicellular eukaryotes, which are categorized into brown, red, or green algae. While brown algae are often the largest in size, red algae have a longer evolutionary history and hence are more diverse. Macroalgae-bacteria relationships have evolved since the first red alga originated about 1.6 billion years ago[2]. In this relationship, the macroalgae is considered to be the host as it is the largest in size. Meanwhile, the microbiome, which is the genetic information of all the microbiota associated, is highly diverse, varying even within the same macroalga species[3][4]. Most macroalgae live in coastal areas, and similar to other marine photoautotrophs, they are mainly found in the euphotic zone. Often, multiple species of algae coexist in close proximity, suggesting overlap in their roles as microbial hosts.

Symbiosis

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Macroalgae are susceptible to symbiosis with microorganisms, as they provide organic material and live in habitats where competition for space is high for benthic organisms[3][5]. The microbiome plays a significant role in the life history of macroalgae with respect to nutrient exchange and reproduction among other functions[4][6]. The symbiosis between epiphytic bacteria and their algal hosts is well documented; the bacteria facilitate metabolic processes in photosynthesis and the nitrogen cycle in exchange for a growth medium[7]. The organic materials secreted by macroalgae provide nutrients for bacterial growth, as well as the formation of marine biofilms[4]. These biofilms act as a barrier between macroalgae and the environment, and provide protection against heavy metals and ultraviolet radiation[8]. Additionally, the bacteria secrete antibiofouling chemicals and prevent colonization by other microbes[3]. However, there is evidence that bacterial biofilms can also be deleterious to macroalgae. A study of Gracilaria, a widely distributed red alga, found that 29% of epiphytic bacterial colonizers contributed to necrosis in tips of the alga[9]. As well, a study on the red alga, Delisea pulchra, found that some viruses within their microbiome infected diatoms, serving as part of the host’s immune system, others induced lysis of host cells[10]. Lastly, stress of the host organisms can lead to disturbances in the microbiome, which can cause mutualistic or commensal bacteria to take advantage of the nutrients released to cause damage to the host[4][11][12].

These complex interactions have evolved from the varying allocation and concentration of chemical compounds, as they are crucial for communication between aquatic organisms[3][13]. The most well-documented chemical compounds are antibacterial in nature, whether they are produced by the microorganisms or the alga themselves. In the case of the alga, there is evidence that the red macroalga Gracilaria textorii is able to secrete chemical substances to control the populations of Vibrio alginolyticus and Vibrio logei[14]. Meanwhile, 35% of epibiotic bacteria in Scottish coastal waters and 20% epibiotic bacteria in Japan waters were found to secrete antimicrobial compounds[15][16]. Those compounds are found to target or have antibiofouling properties against a very wide range of other microorganisms[15][17]. As a result of those chemical interactions, certain bacteria can be found in specific macroalgal species[3]. It is also found that the microbial communities in the same species under different habitats are more similar than the communities in different species under the same habitat[18].

Microbial Community Composition

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Sphingomonas phyllosphaerae, a common bacteria found on the macroalgae Gracilaria vermiculophylla.

The composition of a macroalgal microbial community is highly host-specific; it not only varies between species, but even among species in different locations[4][19]. For example, a study of Ulva intestinalis, Fucus vesiculosus and Gracilaria vermiculophylla (green, brown, red algae respectively) found minimal overlap in epibacterial community composition[20]. Although these three species are highly widespread and abundant, their evolutionary histories differ considerably, leading to different ecological niches. In particular, shared dominance between Rhizobiales and Bacteroidetes was observed on G. vermiculophylla, indicating a preference for nitrogen fixers. Meanwhile, on U. intestinalis, populations of Sphingomonadales was found to predominate in the summertime, and Bacteroidetes in the other seasons[20]. Again, Bacteroidetes made up a significant portion of the microbial community on F. vesiculosus in all seasons. Overall, since Bacteroidetes is known to promote nutrient cycling and defend against abiotic stressors, it is a core and ubiquitous component of the macroalgal holobiont in a variety of algae species[21]. At the same time, populations of Verrucomicrobia, which contribute to the degradation of fucoidan, were found to spike in the summertime on brown algae[22]. This may suggest temperature requirements for certain bacteria to grow on their algal hosts.

The primary means of classifying bacteria is through culturing a sample on a growth medium, which can be either solid or liquid. However, this approach isn’t sufficient in the context of the macroalgal microbiome, since only a small fraction of microbes can grow in those laboratory conditions (estimates concur on a value of less than 1%)[23]. More recently, gene sequencing techniques using samples taken directly from biomass have been developed; though this is an advancement, much of the microbiome still remains unknown. This was exemplified in a 2010 study on various species of Ulvaecean algae. Pseudoalteromonas is known to exist in symbiosis with Ulva, primarily to help prevent biofouling[24]. However, when using community profiling techniques, Alphaproteobacteria was identified as the primary bacterial group – the authors noted that other bacteria such as Pseudoalteromonas had been consistently found in past studies but missed with their methods[23][25]. For this reason, the holistic understanding of all microbial interactions in the holobiont remains limited.

Functions

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Morphogenesis

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Bacterial members of the macroalga microbiome have been shown to have a morphogenetic effect on the host[26]. Early studies have shown that the axenic Ulva lactuca cannot develop the typical foliaceous thallus, but instead, they grow into filamentous or finger-like germlings which are capable of originating new germlings upon disintegration or transfer after growing a few millimeters [27][28]. However, in some green algae species, it has been shown that the typical foliaceous morphology could be regained upon reinfection of certain marine bacteria isolated from marine macroalgae, seawater and coastal sediment. In addition, Monostroma species could even restore their typical morphology with the filtrates of appropriate bacterial cultures, which further prove the morphogenetic effect of bacterial members of macroalga microbiome[29][30]. Later studies characterized the inducers for such macroalgae morphogenesis or redifferentiation. For instance, thallusin, which was isolated from an epiphytic bacterium in the Cytophaga-Flavobacterium-Bacteroides group from Monostroma sp., could induce the differentiation of Monostroma oxyspermum and germination of other green macroalgae (U. pertusa and E. intestinalis)[31]. Moreover, several bacterial species isolated from the microbiome of Ulva. mutabilis excrete cytokinin-like and auxin-like regulatory factors, which affect the development and differentiation of host gametes[32].

Reproduction

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Chemical structure of N-acyl homoserine lactones, a quorum sensing signal.

Quorum sensing (QS) is a mechanism of intercellular communication that shares the information about cell density among a bacteria community. This density-dependent communication is done by production and detection of signaling molecules and it allows bacteria to regulate gene expression of certain processes cooperatively[33][34]. Bacterial members of the macroalgae microbiome have been shown to chemically communicate through QS, and relevant QS molecules could potentially influence the host reproductive cycle[26]. For instance, certain Gram-negative bacteria species isolated from green algae (Ulva fasciate and Ulva lactuca) and red algae (Gracilaria corticate and Gracilaria dura) produce various types of N-acyl homoserine lactones (AHLs) as quorum sensing signal molecules. Some of these AHLs were shown to promote carpospore liberation from G. dura[35].

Health

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Surface microbiome of the macroalgae play an important role in regulating the health condition of the host. Host-specific bacteria colonization could be selected by the nutrient source available on the surface or exudates[4]. Bacteria are shown to be partly responsible for the production of specific vitamins required by different macroalga species and some antimicrobial compounds against pathogens, which were known to be produced by seaweeds[36].

On the other hand, the symbiotic relationship of the macroalga microbiome with their host could shift to a potentially pathogenic relationship upon spatial or temporal shifts of the macroalga microbiome. This can be caused by abiotic challenges (e.g., environmental conditions change) and/or biotic challenges (e.g., host physiology change)[4][37]. Such shifts of the microbiome from “stable state” to “disturbed state” are referred to as dysbiosis, under which commensal or new colonizers could become opportunistic pathogens. A study has shown that the fronds surface microbiome of the giant kelp, Macroxystis pyrifera, was influenced by global climate change stressors (e.g., increased temperature and pCO­2). In addition, the unique shift in the M. pyrifera surface microbiome was correlated with reduced growth of the host, which was proposed to be associated with the increase in Flavobacterales species[37]. To add on, several bacterial species isolated from the surface microbiome of Agarophyton vermiculophyllum were classified as “pathogens” and “protective.” Kordia algicida, which was identified as a “significant pathogen” for bleaching disease, was also isolated from the Agarophyton vermiculophyllum surface. When all the isolates were tested together, the protective strains seem to completely prevent bleaching disease. However, such common presence of pathogens in the surface microbiome suggests the possibility of pathogenesis upon environmental stress or other disturbances[38]. Moreover, a morphological disease affecting red macroalga Iridaea laminarioides, that is characterized by gall development on immature thalli, was shown to be associated with infections of an endophytic cyanobacterium. This study was the first report of association between macroalgal disease and endophytic organisms[39].

Surface Defence

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Some symbiotic members of the macroalga microbiome play an important role in assisting chemical defences of the host against foulers and pathogens[4]. It has been demonstrated that macroalga holobiont, Agarophyton vermiculophyllum, possesses a beneficial microbiome on the surface that produces metabolites to reduce colonization of opportunistic pathogens and attract “protective epibacterial settlement”. As introduced previously, when all the isolates of Agarophyton vermiculophyllum (including both protective and pathogenic strains) were tested together, the bleaching was fully prevented by the protective strains. This suggests that Agarophyton vermiculophyllum’s surface microbiome demonstrates an “associational defence” against pathogens[38]. Furthermore, bioassays have proven that the selective recruitment of microbes on Agarophyton vermiculophyllum surface is chemically mediated, where surface metabolites attract protective strains and reduce settlement of pathogens. This was the first demonstration of the capacity of an aquatic macrophyte to chemically “garden” beneficial microbiome for better disease resistance[38]. In addition to bacterial colonizers, a few surface bacteria strains of different macroalgae species have also demonstrated slight to strong inhibitory effect against settlement of tubeworm larvae and algal spores[40]. Moreover, different macroalgal surface bacteria isolates were also shown to exhibit antibiotic properties against other bacteria, prevent fouling of pennate diatoms and even reduce barnacle attachment[41][42]

Applications

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Macroalgal microbiome offer extensive potential in the fields of science and technology. Due to its unique properties, the microbiome has been applied to several studies including climate crisis mitigation through carbon sequestration, halogen metabolism in the marine halogen cycle, biofuel production, and environmental remediation[43][44][45].

Carbon Sequestration

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A simple model of carbon sequestration.

The cultivation of large seaweeds is gaining significant attention for its potential in climate change mitigation. This interest is due to macroalgae's substantial contribution to ocean carbon sequestration[43]. Refractory dissolved organic carbon (RDOC), which makes up 96% of the marine dissolved organic carbon (DOC) pool, is created by bacteria eating the labile components of DOC from primary producers[43]. The term "refractory" is used to characterize this DOC pool because a significant portion of it appears to be "non-accessible" or "resistant" to fast microbial breakdown. Because of this, RDOC is considered an important carbon reservoir that can effectively slow down global warming. Macroalgal species like Sargassum and Ulva prolifera have also shown strong environmental adaptability. These species absorb considerable amounts of CO2 from the atmosphere and nutrients from seawater, and thus have a significant role in carbon sequestration[43]. However, these algae blooms can also have negative impacts, such as coastal hypoxia and acidification, due to the degradation of these macroalgae by microbes[46].

Halogen Metabolism

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Microbes of red and brown algae in particular play a crucial role in the halogen cycle found in marine ecosystems[47]. The algae host a variety of microbial populations that make halogenated compounds, a crucial field of research for future biotechnological and ecological uses[44]. Little is known as to why microbiomes produce halogenated compounds, with some suggesting antimicrobial functions in interactions between macroalgae and prokaryotes[44]. The research is focused on understanding the genetic make up of prokaryotic communities associated with macroalgae, and how this influences reactions with organohalogenated molecules in the ocean[44]. The findings point at macroalgae functioning as holobionts. The metabolism of halogenated compounds by macroalgal microbiomes might play a role in symbiogenesis and act as a possible defense mechanism against chemical stressors in the surrounding environment[44].

The study provides insights into synthetic biology by highlighting the gene content in bacterial groups previously unrelated to organohalogen metabolism that is biotechnologically relevant. This study offers useful information that advances the knowledge of the function of unknown prokaryotes in marine ecological interactions[44].

Biofuel

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Microbiomes associated with macroalgae have potential applications in biofuel production through their action in the breakdown of complex sugars[45]. These can be transformed into bioethanol, biogas, biodiesel, and bio-oil using methods such as fermentation, anaerobic digestion, transesterification, and pyrolysis because of the sugar components in macroalgae[45][48]. Saccharina japonica for example, a type of brown macroalgae, contains carbohydrates like alginate, laminarin, and mannitol that can be converted into biofuels. The significant alginate content can be broken down into monosaccharides which are then used to produce ethanol as a biofuel[45]. In red macroalgae, galactose (23%) and glucose (20%) provide the most significant percentages of simple sugars, and co-fermentation is used as the strategy for bioproduction of ethanol. Green macroalgae present with a significant fucose composition, leading to the production of diols when broken down, and 2'-fucosyllactose (2'-FL), a key component of human milk oligosaccharides (HMOs)[49][50]. 2'-FL is especially useful in nutraceutical applications since infant formula made from non-human-animals' milk contains very few oligosaccharides[45]. Microorganisms are key in these processes by breaking down polymers into sugars suitable for use in metabolic engineering technologies.

Bioremediation

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Oil-utilizing bacteria were found immobilized in biofilms coating the thalli of macroalgae in the waters of the Arabian Gulf[51]. These bacteria were shaken in hydrocarbon-containing water and proved increased absorption over a two week period, making phytoremediation as an approach for cleaning oily terrestrial environments plausible in the near future using enhanced macroalgal microbiomes[51].

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