Lactic acid fermentation of Arthrospira platensis (spirulina) biomass for probiotic-based products
Journal of Applied Phycology
https://doi.org/10.1007/s10811-018-1602-3
Lactic acid fermentation of Arthrospira platensis (spirulina) biomass
for probiotic-based products
Alberto Niccolai 1 & Emer Shannon 2 & Nissreen Abu-Ghannam 2 & Natascia Biondi 1 & Liliana Rodolfi 1,3 &
Mario R. Tredici 1
Received: 19 July 2018 / Revised and accepted: 8 August 2018
# The Author(s) 2018
Abstract
The first objective of this study was to evaluate the use of lyophilised biomass of the cyanobacterium Arthrospira platensis F&MC256 as the sole substrate for lactic acid fermentation by the probiotic bacterium Lactobacillus plantarum ATCC 8014. After 48 h of
fermentation, the bacterial concentration was 10.6 log CFU mL−1 and lactic acid concentration reached 3.7 g L−1. Lyophilised A.
platensis F&M-C256 biomass was shown to be a suitable substrate for L. plantarum ATCC 8014 growth. The second objective of the
study was to investigate whether lactic acid fermentation could enhance in vitro digestibility and antioxidant activity of A. platensis
biomass. Digestibility increased by 4.4%, however it was not statistically significant, while the antioxidant activity and total phenolic
content did increase significantly after fermentation, by 79% and 320% respectively. This study highlights the potential of A. platensis
F&M-C256 biomass as a substrate for the production of probiotic-based products.
Keywords Arthrospira platensis . Spirulina . Lactic acid fermentation . Probiotics . Digestibility
Introduction
Lactic acid-fermented products from milk (yogurt and cheese)
are widely consumed, but the demand for dairy-free alternatives is rapidly rising because of the increasing incidence of
lactose intolerance and veganism, and as a response to the
request for higher nutritional quality and fortified food products (Kandylis et al. 2016; Panghal et al. 2018). In this respect,
lactic acid fermentation is considered a valuable technology to
enhance shelf life, safety, sensory and nutritional properties of
vegetables and fruits (Di Cagno et al. 2013).
Some algae represent a suitable substrate for the production of
fermented foods due to their availability and high nutritional value (Gupta and Abu-Ghannam 2011; Gupta et al. 2011; Uchida
and Miyoshi 2013). Many and diverse fermented products (powders, beverages, delicacies) from seaweeds, microalgae (mainly
* Mario R. Tredici
1
Department of Agrifood Production and Environmental Sciences
(DISPAA), University of Florence, Piazzale delle Cascine 24,
50144 Florence, Italy
2
School of Food Science and Environmental Health, Dublin Institute
of Technology, Cathal Brugha St, Dublin 1, Ireland
3
Fotosintetica & Microbiologica S.r.l., Via dei Della Robbia 54,
50132 Florence, Italy
Chlorella and Dunaliella) and spirulina (different Arthrospira
species), usually mixed with plant-derived substrates and obtained through different fermentative processes (by lactic acid bacteria or yeasts or a mixture of these microorganisms), are available
in the market and easily found on e-commerce platforms.
In comparison to the numerous studies on algae fermentation
(Gupta et al. 2011; Nguyen et al. 2012; Talukder et al. 2012;
Uchida and Miyoshi 2013), those on cyanobacteria are limited
and focus particularly on Arthrospira spp. Bhowmik et al.
(2009) added spirulina biomass to cultures of different
Lactobacillus and Streptococcus strains and performed 10h
fermentations, observing an increase in the bacterial number
with increasing biomass concentrations. Parada et al. (1998)
added the filtrate from A. platensis cultures to various lactic acid
bacteria cultures, which were allowed to ferment for 24 h. The
filtrates increased growth of all the bacterial strains. De Caire et
al. (2000) added spirulina biomass at different concentrations to
milk and then fermented the suspension with a blend of lactic
acid bacteria. The presence of spirulina biomass favoured the
growth of the bacteria. Several authors (Varga et al. 2002;
Guldas and Irkin 2010; Beheshtipour et al. 2012, 2013;
Mazinani et al. 2016) have tested the effect of spirulina biomass
addition to yogurt, cheese, and fermented milk, with positive
results, among which included an increase in the number of
lactic acid bacteria and improvement of the nutritional quality
of the fermented product during storage. However, to the best of
our knowledge, the suitability of spirulina biomass as the sole
J Appl Phycol
substrate to obtain lactic acid-fermented products has not been
investigated.
Arthrospira, besides accumulating, like all cyanobacteria,
glycogen as primary energy and carbon reserve, contains high
levels of proteins (up to 70% dry mass) of high value due to the
presence of all the essential amino acids (Becker 2007).
Arthrospira also contains high levels of vitamins, minerals (particularly iron), essential fatty acids (particularly γ-linolenic acid),
carotenoids and chlorophyll (Ghaeni et al. 2014), and a number
of unexplored bioactive compounds (Kulshreshtha et al. 2008;
Tredici et al. 2009; Chacón-Lee and González-Mariño 2010;
Soheili and Khosravi-Darani 2011). Arthrospira has potent antioxidant activity due to the presence of polyphenols and phycocyanin (Liu et al. 2011) and also shows interesting lipid-lowering effects (Colla et al. 2008; Bigagli et al.
2017). Arthrospira nutritional properties could be improved
through lactic acid fermentation, which could increase digestibility of the biomass and availability of nutritious substances,
besides providing probiotic bacteria.
Probiotic microorganisms are Blive microbial food supplements which beneficially affect the host animal by improving
its microbial balance^ (Fuller 1992). Lactobacillus plantarum
has been proposed as probiotic, and several studies have
been performed that show its capacity to resist transit
through the gastric tract, ability to colonise the host gut,
safety and potential health benefits such as cholesterol
reduction (de Vries et al. 2006; Georgieva et al. 2009;
Karczewski et al. 2010).
A prebiotic is defined as Ba substrate that is selectively
utilized by host microorganisms conferring a health benefit^
(Gibson et al. 2017). Polysaccharides from algae, for example
β-glucans from C. vulgaris, and spirulina biomass are already
recognised and accepted as dietary prebiotics (Jiménez-Escrig
et al. 2013; de Jesus Raposo et al. 2016).
This study was designed to investigate the suitability of A.
platensis F&M-C256 biomass as the sole substrate for L.
plantarum ATCC 8014 growth and fermentation and to evaluate the fermented product in terms of probiotic bacteria content, in vitro digestibility and antioxidant capacity, which are
parameters of great importance for the development of functional foods.
Materials and methods
A. platensis F&M-C256 biomass production
Biomass of Arthropira platensis F&M-C256 was produced at
Archimede Ricerche S.r.l. (Imperia, Italy). The cyanobacterium was cultivated in Zarrouk medium (Zarrouk 1966) in
GWP®-I photobioreactors (...truncated)
