Humic Substances as Microalgal Biostimulants-Implications for Microalgal Biotechnology

Abstract

Humic substances (HS) act as biostimulants for terrestrial photosynthetic organisms. Their effects on plants are related to specific HS features: pH and redox buffering activities, (pseudo)emulsifying and surfactant characteristics, capacity to bind metallic ions and to encapsulate labile hydrophobic molecules, ability to adsorb to the wall structures of cells. The specific properties of HS result from the complexity of their supramolecular structure. This structure is more dynamic in aqueous solutions/suspensions than in soil, which enhances the specific characteristics of HS. Therefore, HS effects on microalgae are more pronounced than on terrestrial plants. The reported HS effects on microalgae include increased ionic nutrient availability, improved protection against abiotic stress, including against various chemical pollutants and ionic species of potentially toxic elements, higher accumulation of value-added ingredients, and enhanced bio-flocculation. These HS effects are similar to those on terrestrial plants and could be considered microalgal biostimulant effects. Such biostimulant effects are underutilized in current microalgal biotechnology. This review presents knowledge related to interactions between microalgae and humic substances and analyzes the potential of HS to enhance the productivity and profitability of microalgal biotechnology.

Keywords: enhanced microalgal productivity; higher accumulation of bioactive ingredients; hormetic effects; humic substances; improved protection against abiotic stress; increased nutrient availability; microalgae cultivation.

Figure 1

The mechanisms of humic substances (HS) effects on microalgae cells. HS increase membrane permeability for calcium and ferrous ions and diffuse through the plasmatic membrane. Ferrous ions promote the formation of reactive oxygen species (ROS) by redox reaction and activate the formation of nitric oxide (NO) from polyamines. Calcium ions activate specific protein kinases involved in cellular signaling. Intracellular HS interfere with the electron transport chain in chloroplasts and mitochondria, producing a higher level of reactive oxygen species. The simultaneous increase in NO and ROS levels causes an accumulation of reactive nitrogen species (RNS). The resulting nitrosative stress causes the development of physiological compensation mechanisms, which ultimately lead to the activation of primary and secondary metabolism. An increase in oxidative and nitrosative stress over the physiological thresholds damages cell function. HSPs—thermal shock proteins; MPK6—mitogenically activated protein kinases; CDPK—calcium-dependent protein kinases.

Figure 2

Illustration of the main mechanisms involved in microalgae protection by humic substances and the characteristics that are involved in these mechanisms.

Figure 3

Development of second-generation plant biostimulants based on microalgae bioassay of interactions between humic substances and other active ingredients. The high-throughput screening on microalgae selects a combination with synergic effects that are further verified in plant biostimulant bioassay. Extracts of HS-biostimulated microalgae could be also used in association with the added HS for their activity as plant biostimulants, by using several bioassays—radicular proton pump induction [220], Vicia faba genotoxicity and cytotoxicity test [221], Arabidopsis germination and rosette growth [222], Gibberellic acid-independent amylase activity in barley [223].

Figure 4

Using the humic substances as biostimulants for microalgae in integrated biotechnology, converting by-products from bioeconomy and carbon dioxide from fermentation process into high-value bioproducts—dietary supplements, food and feed additives, plant biostimulants. The complementary or even synergic HS interactions with components from microalgae used as active ingredients in these bioproducts underpin HS utilization as a biostimulant for microalgae.