Microalgae can produce amino acids such as tryptophan, a precursor for auxin biosynthesis in bacteria, promoting mutualistic interactions
[12][13][39,40].
1.2. Oxygen and Carbon Dioxide Exchanges
The co-cultures of bacterium and algae may be effective in detoxifying inorganic and organic pollutants and removing nutrients from wastewater if compared to the activity of these microorganisms individually. Photosynthesis by cyanobacteria and eukaryotic algae provides oxygen, an essential factor for heterotrophic bacteria that degrade pollutants. Sequentially, the bacteria help the photoautotrophic growth of the collaborators, furnishing carbon dioxide and stimulating factors
[14][17] and decreasing the oxygen concentration in the culture medium
[15].
This relationship is interesting because microalgae can be part of a circular economy, since it allows the use of CO
2 coming from industrial processes, like distilleries (CO
2 from alcoholic fermentation and sugarcane bagasse burning), cement industry (CO
2 from burning of energy source and CaCO
3 decomposition), energy industry (CO
2 from burning of energy source) as well as from aerobic and anaerobic treatment of wastewaters, as a carbon source to produce microalgae biomass. Simultaneously, the oxygen produced by phytoplankton may support the necessity of aerobic processes in these industries. The oxygen produced by microalgae could be used in an integrated process involving aerobic depuration of wastewaters, with a production of bacteria which could be used in different applications, like agricultural inoculants, among others, depending on the species of microorganism cultivated
[16][45].
2. Effects of Interactions
2.1. Inhibitory Effect by Metabolites on Algae and Bacteria
Although several species of bacteria have a beneficial effect on algae growth, some bacterial species may also inhibit microalgae by producing extracellular algaecide compounds
[17][22]. This inhibitory effect helps to control the proliferation of harmful algae in bodies of water
[15].
Some bacteria can induce the lysis of microalgal cells. For instance, the
Kordia algicida secretes an algaecide protease that hinders the growth of several diatomaceous marine species
[18][46]. Bacteria can compete with microalgae for limiting nutrients, such as nitrogen and phosphorus, when they grow together in an organic carbon source. Due to the higher growth rate of bacteria than microalgae in this condition, their propagation would consume more nutrients, limiting the growth of eukaryotic photosynthetic microorganisms due to a lack of nutrients
[19][25]. For instance, when
Acinetobacter sp. was inoculated in the exponential phase, a substantial drop in the growth of
Botryococcus braunii was observed. This bacterium, which presented a negative interaction with
B. braunii, produces AHL signaling molecules involved in bacterial quorum sensing, which were found in the non-axenic culture of microalgae
[20][47].
From these considerations, it is important to evaluate the environmental conditions of the processes where the presence of undesirable bacteria is minimized and preferentially suppressed to maximize the microalgal growth. Otherwise, favoring beneficial bacteria within an appropriate threshold is also a determinant for optimizing microalgae growth.
2.2. Bacteria That Promote the Growth of Microalgae
Normally, non-pathogenic bacteria from several species have been found in microalgae cultivations with beneficial effects on their growth.
It has been shown that bacteria may modify the growth of phytoplankton, accumulating biomass and increasing cell productivity, which is of particular interest for industrial production. The bacteria of the genera
Alteromonas and
Muricauda allowed the most significant accumulation of
Dunaliella biomass due to the increase in the availability of nitrogen for microalgae. However, more research is needed to understand the mechanisms behind these interactions
[21][49].
In the cultivation of
Chlorella prototecoides in synthetic wastewater media in co-culture with
Brevundimonas diminuta with light intensities of 75 and 130 μmol photons m
−2s
−1, the μ values in non-axenic conditions were at least five times higher than in cultivations without co-culture. Thus, under these conditions, the addition of
Brevundimonas diminuta was able to provide higher growth rates of
C. protothecoides with more efficient nutrient removal
[22][50].
A substantial promotion in the growth of phytoplankton has been described because the bacterium produces indole-3-acetic acid (IAA)
[15]. The
Achromobacter sp. produces IAA, which promotes the growth of
Haematococcus pluvialis, with an increase in chlorophyll and cell concentrations
[23][51]. In fact, the bacterial population in low concentrations can improve the microalgae metabolism by releasing factors that promote growth or reduce the concentration of O
2 in the medium, preventing this gas from reaching an inhibitory concentration. As a consequence of higher microalgae growth in co-culture with bacteria, there is a higher removal of nutrients from the cultivation medium, which is particularly important in the tertiary treatment of wastewater since nitrogen and phosphorus are constituents of the microalgae biomass. In a study using synthetic wastewater with a semi-continuous process, the immobilized consortium of
Chlorella vulgaris and
Azospirillum brasilense led to an increase in the uptake of ammonium by culture
[24][52]. Thiamine and tryptophan released by
C. sorokiniana are signaling molecules that may be used by
A. brasilense to synthesize and secrete another signaling molecule, indole-3-acetic acid, which promotes microalgae growth. The occurrence of signaling compounds, such as thiamine and tryptophan in the exudates of
Chlorella sorokiniana, supports the mutualistic interaction of this photosynthetic microorganism with
A. brasilense [25][53].
2.3. Supply of Nutrients
Microalgae may increase bacterial activity by secreting extracellular molecules such as lipids, proteins, and nucleic acids that serve as nutrients for bacterial growth. In this sense, dead microalgae cells can also provide nutrients for the growth of bacterial cells
[15].
Croft et al. (2005) showed that vitamin B12 is an important molecule in algae metabolism, the main cofactor for methionine synthase, which depends on vitamin B12. They also observed that cobalamin auxotrophy had appeared numerous times throughout evolution processes, probably related to the presence or absence of vitamin B12-dependent enzymes. An example of this symbiosis is the case of bacteria of the genus
Halomonas, that supply cobalamin for the microalgae
Amphidinium operculatum [26][57].
Pseudomonas sp., on the other hand, produced a glycoprotein that performed as a growth factor for
Asterionella glacialis [27][58]. In another research, the growth of
Chlorella sp was shown to be improved due to the release of riboflavin by
E. coli [28][59].
2.4. Modification of the Composition of Microalgae in Co-Culture
The association of Rhizobium sp. KB10 with B. braunii increased algae growth by nine times and improved the oleate content, used to produce biodiesel [29][61]. Inoculation of the bacterial strain Rhizobium 10II in the cultivation of Ankistrodesmus sp. strain SP2-15 increased by 30% the chlorophyll content in the microalgae biomass, and the lipid productivity was up to 112 g.m−2d−1 on the sixth day of cultivation [30][62]. The co-cultivation of Chlamydomonas reinhardtii with Bradyrhizobium japonicum improved the growth of the microalgae by 3.9 times, reaching lipid contents 26% higher and increasing Fe-hydrogenase activity and H2 production [31][63].
2.5. Flocculant Activity by Bacteria
The activity of bio-flocculant depends on the growth phase of the bacteria, being enzymatic activities related to the formation of bio-flocculants observed during the stationary growth phase. Although the production of bacterial bio-flocculant is beneficial for improving the formation of large flakes of microalgae and bacteria, the additional cost related to the carbon source required for the growth of these bacteria still remains a challenge
[32][67], which evidence that organic by-products could be used to produce such bacteria, thus diminishing the cost of the process
[33][68].
Exopolysaccharides and pyruvic and uronic acids are important for cell adhesion. In addition, factors such as the sources of nitrogen and carbon and the ratio between these two elements influence the production of bio-flocculants. The bio-flocculant produced by the
Paenibacillus polymyxa exhibited high efficiency for the flocculation of
C. vulgaris and
Scenedesmus sp.
[32][67].
Bacteria such as
Flavobacterium, Terrimonas, and
Sphingobacterium and their extracellular polymeric substances may help to increase the flocculating activity of algae such as
C. vulgaris, resulting in sedimentable flakes
[34][69].
2.6. Microalgae Co-Immobilization by Bacteria
Microalgae are part of the organisms attached to filters in wastewater treatment plants, where the wastewater percolates during the treatment process. In these filters, enzymes or whole cells may be immobilized, including microalgae cells, which serve to obtain more biomass and for removing macronutrients since the production of oxygen by the algae improves the aerobic degradation of these substances. Moreover, the consumption of CO
2 and the production of exopolysaccharides by microalgae can increase the bacterial growth rate, as CO
2 and the production of growth-promoting substances by bacteria can improve microalgae growth. However, bacteria and microalgae may produce substances that hinder the growth of the other co-immobilized organism. Besides, the increase in pH and oxygen concentration in the medium, due to photosynthetic activity, can reduce bacterial growth in the system with the co-immobilization of bacteria and algae
[35][70].
3. Microalgae as Potential Raw Material for Bioproducts
Considering the information on the interaction of microalgae and bacteria, besides the high potential of using microalgal biomass as a source of carbohydrates or fatty acids for energy production, food, cosmetic, and pharmaceutical industries, one could develop products in which microalgae, or their components could be used to confer special properties to them (
Figure 12).
Figure 12.
Diagram about how the study of microalgae-bacteria interactions can result in bioproducts.
3.1. Extracts for Microbial Growth
Considering that bacteria and microalgae are rich in valuable organic compounds, and considering the related well-succeeded co-culture between these organisms, their extract could improve their growth. In this approach, Carvalho et al. (2021) developed a bacterial extract to promote the cultivation of microalgae, providing important nutrients for their growth. This extract allows greater growth in axenic and non-axenic strains of
Dunaliella salina and non-axenic strains of
Chlorella vulgaris [33][68].
3.2. Bioproducts
3.2.1. Microalgae for Developing Prebiotic Products
It is possible to develop foods based on the interactions between microalgae and bacteria, such as those that are not digestible, to beneficially affect the host by stimulating proliferation or activity of populations of beneficial bacteria in the intestine. There was a positive effect of
Arthrospira on bacteria in the intestine, increasing the growth rate of
Lactobacillus, thus supporting the function of the digestive tract and being used as a prebiotic
[36][73].
3.2.2. Animal Diet
Cerezuela et al. (2012) carried out in vivo studies of experimental diets with
Tetraselmis chuii (T),
Phaeodactylum tricornutum (P) and
Bacillus subtilis (B), simple or combined, showing morphological changes and significant signs of intestinal damage. The diets applied to fish led to a decrease in the bacterial diversity in the intestinal microbiota. Only diets containing
Bacillus subtilis resulted in a significant reduction in the height of the microvilli. Moreover, fish fed with experimental diets showed different signs of edema and inflammation, and the
scautho
lars concluded that such effects could compromise fish body homeostasis
[37][79]. These findings highlight the necessity of evaluating, case by case, the benefits and risks of including any microorganism in animal and human diets.
3.3. Cosmetics
The growing need for obtaining safe products by bioprocesses has made microalgae a sustainable source for new products. Currently, microbial sources are the best available on the market to replace implemented entities
[38][82].
Several secondary metabolites produced by algae are known to benefit the skin. Algae cells are naturally exposed to oxidative stress, which makes them develop efficient protection systems against radicals and reactive oxygen species, producing biomolecules that may act in cosmetics against the damaging effects of UV radiation, promoting the same action of inorganic filters and organic agents currently commercialized. There is an increase in the production of carotenoids and chlorophyll by
Chlorella vulgaris, Arthrospira, and
Nostoc when growing in the presence of radiation. These biomolecules can help to protect against the oxidative process of oil in formulations, especially in emulsions with a large quantity of oily phase, as they have antioxidant activities
[39][83]. Such properties of microalgae can be used for the development of sunscreens, being associated with the formulation or the skin.
Due to the fact that biofilm is related to infections, particularly due to the low susceptibility of microorganisms to traditional antimicrobial agents, microalgae may be explored seeking an innovation to solve this problem. The antibiofilm activity of
Arthrospira platensis extracts, which are abundant in free fatty acids, was verified. The nanocarriers based on copper alginate loaded with extract, were able to inhibit the formation of biofilms from one and two species of
Cutibacterium acnes, but did not inhibit preformed biofilms. Nanovectorized extracts reduced the growth of
Candida albicans biofilms, as well as preformed biofilms
[40][84].
3.4. Pharmaceuticals
Currently, resistant strains are gaining attention in the treatment of bacterial infections
[41][10]. Therefore, a new strategy is oriented, using a chemically modified
Chlamydomonas reinhardtii as a drug delivery system. These modified microalgae masked vancomycin thanks to an insertion of a photocleavable binder on the cell surface, and the antibiotic was released in a controlled way, under exposure to ultraviolet light (340–400 nm). This technique was tested on
Bacillus subtilis, successfully resulting in growth inhibition of this bacterium
[42][86]. Microalgae, as earlier commented, can produce compounds that lead to the inhibition of bacteria, which can be extended to other microorganisms and even viruses
[43][87].