Bacterial Enhancement of Microalgal Metabolite: Comparison
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Microalgae are photosynthetic microorganisms with a high potential to produce a wide variety of industrial-interest metabolites such as proteins, lipids, carbohydrates, and pigments. 

  • mutualism
  • microalgae
  • growth-promoting bacteria
  • metabolites
  • biorefinery

1. Introduction

Microalgae are photosynthetic microorganisms with a high potential to produce a wide variety of industrial-interest metabolites such as proteins, lipids, carbohydrates, and pigments. Their rapid growth rates and the possibility to be cultivated on nonarable land constitute an advantage against plant-based sources [1].

Overproduction of microalgal metabolites has been optimized by several mechanisms, from the alteration of culture conditions (nutrient concentrations, light intensity, carbon source, salinity, and temperature) to metabolic engineering [2][3][4][5]. Another way to stimulate metabolite production is through the application of chemical triggers, such as phytohormones and analogs regulating microalgal metabolism, or of chemicals that can regulate biosynthetic pathways, induce oxidative stress responses, or act directly as metabolic precursors [6][7][8]. Since these growth-promoting factors are produced by bacteria, microalgae–bacteria consortia have been explored as an alternative route to enhancing microalgae growth and metabolite production [9][10].

Microalgae and bacteria have coexisted since the early stages of evolution. From a biotechnological aspect, the symbiotic interactions cover a wide range, mostly mutualistic, commensalistic, or parasitic [11]. Mutualisms are positive interactions among different species that improve the fitness of the involved partners and are based on the exchange of resources and services [12][13]. A mutualistic microalga–bacteria consortium is based on the exchange of metabolites, mostly the bacterial uptake of extracellular organic carbon released from the algal photosynthesis; in return, the bacterial growth can be stimulated by (1) the removal of oxygen and the generation of carbon dioxide, (2) the supply of nutrients, vitamins, and trace elements for microalgal growth, and (3) the production of growth-promoting factors as well as chelators and phytohormones [14].

2. Enhancement of Biomass and Metabolite Production

The noteworthy increase in microalgae biomass production as a result of co-cultivation with bacteria has driven the study of these mutualistic interactions to boost the production of several microalgae of commercial interest (Table 1).

Table 1. Microalgal growth promotion of some artificial microalgae–bacteria consortia.

Bacteria Microalgae Growth Promotion Effect Culture Medium Reference
Azospirillum brasilense Cd Chlorella sorokiniana UTEX 2714 11% increase in cell density (g dw/L) N8 medium [15]
Azospirillum brasilense Cd A. protothecoides UTEX 2341 90% increase in cell density (g dw/L) N8-NH4
Brevundimonas sp. Chlorella ellipsoidea UTEX 247 50-fold increase in cell density (cel/mL), longer exponential phase Modified BBM [16]
Pelagibaca bermudensis KCTC 13073BP Tetraselmis striata KCTC1432BP 2-fold increase in biomass productivity (mg/L/d) O3 medium [17]
Azospirillum brasilense Cd Chlorella vulgaris UTEX 2714 16 and 11% increase in cell density (cel/mL) and growth rate, respectively Synthetic growth medium (SGM) [18]
Azospirillum brasilense Cd Chlorella sorokiniana UTEX 2805 40 and 35% increase in cell density (cel/mL) and growth rate, respectively
Bacillus pumilus ES4 Chlorella vulgaris UTEX 2714 1.5-fold increase in cell density (cel/mL) N-free SGM [19]
Escherichia coli ATCC 25922 Chlorella minutissima UTEX 2341 3.5-fold biomass productivity (mg/L/d) N8-NH4, 1% Glucose [20]
3.4-fold biomass productivity (mg/L/d) N8-NH4, 1% Glycerol
7.2-fold biomass productivity (mg/L/d) N8-NH4, 1% Acetate
Rhizobium sp. 10II Ankistrodesmus sp. SP2-15 29% increase in dry weight (mg/L) BG11 medium [21]
Stenotrophomona smaltophilia Chlorella vulgaris 22, 20, and 18% increase in biomass (g/L), growth rate and productivity (mg/L/d), respectively BG11 medium [22]
Azospirillum brasilense Cd Chlorella vulgaris UTEX 395 62% increase in cell size Synthetic wastewater [23]
Azospirillum brasilense Cd Chlorella vulgaris UTEX 2714 3-fold increase in cell density
Azospirillum brasilense Cd Chlorella sorokiniana UTEX 1602 2.2-fold increase in cell density
Rhizobium sp. Botryococcus braunii 55% increase in optical density Modified Jaworski

medium		 [24]
Muricauda sp. Dunaliella sp. 7% increase in cell biovolume Modified Walne’s

medium		 [25]
Dinoroseobacter shibae Thalassiosira

pseudonana		 35% increase in cell density SW+ medium [26]
Phaeodactylum tricornutum Stappia sp. 72% increase in cell density F/2 medium [27]
Alteromonas sp. Isochrysis galbana 52% increase in cell density Zobell Marine Broth [28]
Labrenzia sp. Isochrysis galbana 71% increase in cell density

Some of the first studies have been focused on the synthetic mutualism described earlier between Chlorella co-cultivated with A. brasilense. These studies have described the positive effects on microalgae growth derived from this association, such as significant increments in cell size, biomass, growth rate, and productivity [18][23][29]. In other studies, the bacteria selected for co-cultivation have been isolated from wastewater effluents or the surrounding medium of the target microalgae species. For instance, Toyama et al. [30] found that growth-promoting bacteria were ubiquitously present in a wide variety of wastewater effluents. These isolated bacteria promoted cell growth of three different algae strains (C. reinhardtii, C. vulgaris, and Euglena gracilis), enhancing microalgal growth up to 2.8-fold. On the other hand, the bacteria Pelagibaca bermudensis isolated from the phycosphere of Tetraselmis striata enhanced two-fold the biomass productivity of this microalga [17], while population growth was 0.5–3 times higher in Chlorella ellipsoidea, with eight bacterial strains isolated from a long-term culture of C. ellipsoidea [16]. Growth-promoting bacteria were also found by Lee et al. [31] in the phycosphere of Haematococcus pluvialis. The authors reported an increase in H. pluvialis growth at all growth stages, due to high auxin production by co-cultivation with the isolated strain Achromobacter sp. CBA4603. Similarly, the co-cultivation of four bacterial strains (Flavobacterium, Hyphomonas, Rhizobium, and Sphingomonas) isolated from C. vulgaris increased the microalgal population by more than 100% when compared to axenic cultures [32]. Likewise, the growth-promoting effect of the marine bacterium Flavobacterium sp. was evaluated in three marine microalgae (Chaetoceros gracilis, Isochrysis galbana, and Pavlova lutheri). The results revealed that the bacterium enhanced the specific growth rate and maximal density of C. gracilis and kept longer the exponential growth phase of I. galbana and P. lutheri [33].

The cultivation of microalgae with growth-promoting bacteria results not just in the enhancement of biomass production but also in the increment of the intracellular levels of lipids, carbohydrates, pigments, and proteins (Table 2). Most of the recent studies on artificial microalgal–bacterial consortia are focused on lipid content, due to the increasing interest in biofuels and biodiesel production. The studies show that this kind of microbial association improves both lipid productivity and lipid quality for biodiesel production. For instance, lipid accumulation in the microalga C. reinhardtii was significantly improved by co-cultivation with Azotobacter chroococcum under nitrogen starvation [34]. The authors reported an increase of 2.4 times in lipid content and 5.9 times in lipid production with the co-culture and up to 19.4 times the lipid productivity compared with the axenic microalga. This increment was explained by an increase in the levels of expression of genes that positively regulated lipid metabolism, while the expression levels of genes that negatively regulated lipid metabolism decreased. Similarly, Leyva et al. [35] found that the activity of acetyl-CoA carboxylase (ACCase) is enhanced by the co-cultivation of C. vulgaris with the MGPB A. brasilense under autotrophic and heterotrophic conditions. However, although higher levels of lipids were found in co-cultures (up to a five-fold increase under autotrophic conditions), the authors did not find a direct link with the increase on ACCase activity. Likewise, the total content of C16 and C18, which are the main fatty acids present in biodiesel composition, can increase in symbiotic co-cultures. Xue et al. [34] reported more than 80% content of C16 and C18 in the fatty acids produced by the microalga C. vulgaris when cultivated with Stenotrophomonas maltophilia as well as an increase of up to 5% when compared to axenic cultures. Similar results were reported by de-Bashan et al. [23] with the cultivation of three different Chlorella strains with A. brasilense immobilized in alginate beads. Immobilization has been found to maintain the close physical proximity of the two microorganisms to facilitate interaction and avoid external interference from bacterial contaminants [36]. In all the co-cultures, the concentration and variety of fatty acids increased, reaching up to eight different fatty acids in microalgae co-immobilized with the MGPB in comparison to four to five in microalgae-only immobilized cells.

Table 2. Metabolite production enhancement of some artificial microalgae–bacteria consortia.

Bacteria Microalgae Metabolite Production Enhanced Culture Medium Reference
Escherichia coli ATCC 25922 Chlorella minutissima UTEX 2341 6.2-fold lipid productivity (mg/L/d) N8-NH4, 1% Glucose [20]
18.8-fold starch productivity (mg/L/d)
1.8-fold lipid content (%)
5.4-fold starch content (%)
3.1-fold lipid productivity (mg/L/d) N8-NH4, 1% Glycerol
9.9-fold starch productivity (mg/L/d)
2.9-fold starch content (%)
8.2-fold lipid productivity (mg/L/d) N8-NH4, 1% Acetate
27.1-fold starch productivity (mg/L/d)
3.7-fold starch content (%)
Azotobacter chroococcum No 1.0233 Chlamydomonas reinhardtii cc849 2.4-fold lipid content (%) N-free TAP medium [34]
5.9-fold lipid production (mg/L)
19.4-fold lipid productivity (mg/L/d)
Stenotrophomona smaltophilia Chlorella vulgaris Lipid increase by 8–34% BG11 [22]
Phaeodactylum tricornutum Stappia sp. 172% increase in fucoxanthin F/2 medium [27]
    144% increase in chlorophylls    
Phaeodactylum tricornutum Marinobacter sp. 50% increase in total lipids F/2 medium [37]
Rhizobium sp. 10II Ankistrodesmus sp. SP2-15 39% increase in chlorophyll a BG11 [21]
Methylococcus capsulatus Chlorella sorokiniana 42% increase in carbohydrates Industrial wastewater with synthetic biogas as methane source [38]
Methylococcus capsulatus Chlorella sorokiniana 15% increase in lipid content
Azospirillum brasilense Cd Chlorella sorokiniana UTEX 1602 1.6-fold chlorophyll a (µg/g cells) Synthetic Wastewater [23]
1.6-fold chlorophyll b (µg/g cells)
1.7-fold lutein (µg/g cells)
2.5-fold violaxanthin (µg/g cells)
5.5-fold lipid content (µg/g dw)
Azospirillum brasilense Cd Chlorella vulgaris UTEX 395 1.6-fold chlorophyll a (µg/g cells)
1.8-fold chlorophyll b (µg/g cells)
1.8-fold lipid content (µg/g dw)
Azospirillum brasilense Cd Chlorella vulgaris UTEX 2714 2.8-fold chlorophyll a (µg/g cells)
2.5-fold chlorophyll b (µg/g cells)
2.3-fold lutein (µg/g cells)
1.5-fold violaxanthin (µg/g cells)
3.9-fold lipid content (µg/g dw)
Azospirillum brasilense Cd Chlorella vulgaris UTEX 2714 1.4-fold chlorophyll a (µg/g cells) Synthetic Wastewater [39]
2.8-fold chlorophyll b (µg/g cells)
2.9-fold ß-carotene (µg/g cells)
2.5-fold lutein (µg/g cells)
2.3-fold violaxanthin (µg/g cells)
Phyllobacterium

myrsinacearum		 Chlorella vulgaris UTEX 2714 1.8-fold chlorophyll b (µg/g cells) Synthetic Wastewater [40]
1.8-fold ß-carotene (µg/g cells)
2-fold lutein (µg/g cells)
2.2-fold violaxanthin (µg/g cells)
Azospirillum brasilense Cd Chlorella sorokiniana UTEX 2714 3-fold chlorophyll a (µg/mg dw) N8 medium [15]
5-fold chlorophyll b (µg/mg dw)
2.5-fold soluble protein (%)
Azospirillum

brasilense Cd		 A. protothecoides UTEX 2341 40–60% increase in soluble protein N8-NH4

Although less attention has been paid to the production of microalgal pigments, carbohydrates, and proteins by co-cultivation with bacteria, a few studies have also revealed the ability of these bacteria to promote the production of these metabolites in microalgae. For instance, the cultivation of A. brasilense with the microalgae S. obliquus, C. vulgaris, and C. reinhardtii under high CO2 concentrations, as discussed earlier, significantly enhanced microalgal growth as well as metabolite accumulation on each microalga. The authors reported an increase of carbohydrates, proteins, and lipids under all gas mixtures evaluated [41]. Higher levels of microalgal carbohydrates have also been reported as a result of co-cultivation with bacteria. Higgins and VanderGheynst [20] reported significant increments in the starch produced by Chlorella minutissima when co-cultured with E. coli under mixotrophic conditions (glucose, glycerol, and acetate substrates). At 1% substrate concentration, the total starch productivity as well as lipid productivity increased in all the co-cultures compared to axenic conditions. The co-cultivation of two Chlorella strains (C. vulgaris and C. sorokiniana) with A. brasilense supports the positive effect of the bacteria on carbohydrate production of this microalgae genus [18][29]. In these studies, the authors reported up to 72% and 90% increments, respectively, in total carbohydrates of C. vulgaris under autotrophic and heterotrophic conditions, while C. sorokiniana had an increase in carbohydrate production of around 55% under autotrophic conditions and 21% under heterotrophic conditions.

Similarly, microalgal pigment production can be significantly enhanced by co-cultivation with bacteria. Gonzalez-Bashan et al. [40] found that the production of chlorophyll, ß-carotene, lutein, and violaxanthin increased significantly in the microalga C. vulgaris when grown with Phyllobacterium myrsinacearum co-immobilized in alginate beads. A similar study was carried out with A. brasilense, enhancing even more the pigment production of C. vulgaris. The co-immobilization of the microorganisms resulted in increments of up to 35% in chlorophyll a, 176% in chlorophyll b, 186% in ß-carotene, 152% in lutein, and 129% in violaxanthin [39]. Likewise, a significant increase in these four pigments was observed in the microalga C. sorokiniana when co-immobilized in alginate beads with A. brasilense [23]. The use of growth-promoting bacteria to enhance pigment production has great commercial potential, considering the increasing consumer demand for natural products, including the replacement of commonly used synthetic pigments for pigments derived from natural sources [42].

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