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Biopreservatives from yeasts with antimicrobial activity against common food, agricultural produce and beverage spoilage organisms

M. Mewa-Ngongang1, 2,*, S.K.O. Ntwampe1, H.W. du Plessis2, L. Mekuto1 and N.P. Jolly2 1Bioresource Engineering Research Group (BioERG), Department of Biotechnology, Cape Peninsula University of

Technology, P.O. Box 652, Cape Town, 8000, South Africa 2ARC Infruitec-Nietvoorbij (The Fruit, Vine and Wine Institute of the Agricultural Research Council), Private Bag x5026,

Stellenbosch, 7599, South Africa

There are safety concerns regarding the use of chemical food preservatives for reducing microbial contamination in processed foods and post-harvest agricultural produce, and these concerns require a bioprospecting approach. Yeasts produce antimicrobial compounds, but these compounds are not being produced nor used on a large scale due to inadequate development and understanding of process engineering systems that are required for their production. This chapter focuses on bioprospecting of yeasts with the potential to produce antimicrobial compounds. This is a mini review on the current potential of yeasts to produce antimicrobial compounds and some results from research that was conducted. This review will attempt to address the gaps found in the current literature, and to open windows for future research on biopreservatives. A model study of growth and antimicrobial compound production kinetics from Candida pyralidae KU736785 was carried out. Results showed the potential of C. pyralidae as post-harvest biocontrol agent and as a producer of biopreservation compounds. There was a broad-spectrum antimicrobial activity shown against Botrytis cinerea, Brettanomyces bruxellensis and Candida guilliermondii by the C. pyralidae strain including extracts studied. Furthermore, a new concept for quantification of biopreservation activity was established to describe the efficacy of the crude biopreservatives extract.

Keywords: Biopreservation compounds; inhibitory activity; antimicrobial quantification; Candida pyralidae

1. Introduction

As living organisms, spoilage microorganisms also require nutrients for their growth and proliferation [1]. Food, fruits and value added beverage products are usually sources of nutrients for wanted and unwanted microorganisms [2]. It is critical for the food and beverage industries to ensure that products destined for both local and export markets meet stringent quality and regulatory requirements. These products need to be of high quality and with a considerable shelf-life. It is therefore, vital to maintain their quality characteristics as defined by quality standards and/or legislated requirements (both local and international). This can only be achieved by preservative supplementation or post-harvest control methods, which minimises the alteration of product properties and health related hazards to consumers. Microbial spoilage has been reported to be one of the leading factors responsible for food, fruit and beverage losses, and this impacts negatively on the economy of the producing countries [3]. Depending on the produce type, producers are currently using synthetic chemicals as mitigation measures for such losses. Benzoic, lactic, sorbic and acetic acids are some of the major organic acids that have been used in food preservation. These compounds act against a variety of spoilage microorganisms including some fruit spoiling fungal pathogens [4,5]. In post-harvest control of fungi, triazoles, hydroanilide fenhexamid, dicarboximides and succinate dehydrogenase are used [6,7]. Although the use of chemical preservatives has only partially assisted in reducing product losses associated with microbial spoilage, their use in certain instances can cause the deterioration of human organs such as the heart and lungs, and can lead to respiratory diseases, and allergic reactions [8,9]. Contamination in some food and beverage industries is attributed to Dekkera bruxellensis, Dekkera anomala, Zygosaccharomyces bailii, Hanseniaspora uvarum and Candida guilliermondii yeasts species [10-12]. On cereal grains and fruits, spoilage is usually attributed to fungal pathogens belonging to the genera of Botrytis, Fusarium, Penicillium, Aspergillus and Monilinia [13-15].

2. Bioprospecting: Yeasts and their metabolites as potential alternative to synthetic chemicals

Microorganisms such as yeasts that produce growth inhibition metabolites present a biological alternative for food, fruits and beverage preservation. For instance, Candida pyralidae, Kluyveromyces wickerhamii, Kluyveromyces phaffi, Tetrapisispora phaffii, Candida tropicalis, Williopsis mrakii, Hanseniaspora uvarum, Debaryomyces hansenii, Pichia anomala and Pichia fermentas are yeasts that have been reported to produce growth inhibition compounds that act against spoilage fungi and yeasts (see Table 1 and 2). Growth inhibition activity can be attributed to the production of extracellular metabolites, proteins, glycoproteins and volatile organic compounds [16-18]. Some yeasts have competitive growth inhibition characteristics when cultured with other microorganisms, using space colonisation and

Antimicrobial research: Novel bioknowledge and educational programs (A. Méndez-Vilas, Ed.)

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higher nutrients utilisation rate as primary mechanism of inhibition [19-24]. The biochemistry of the antimicrobial agents have been found to be strain dependent [25-28]. Biocontrol of fungal pathogens using metabolites produced from yeasts, is achieved by the suppression of β-glucan synthesis or hydrolysis of β-glucan in the cell wall of spoilage organisms. Some control mechanisms inhibit DNA synthesis, which blocks cellular division, thus preventing the proliferation of spoilage organisms. Other modes of action include the cleavage of the tRNA as well as interference with the uptake of calcium and the formation of ion-leaking channels on the cytoplasmic membrane, culminating in cell deactivation [29-31]. In addition, there are other growth inhibitors such as antifungal hydrolases, bacterial pigments that cause iron depletion in spoilage organisms; antimicrobial peptides, β-lactam antibiotics, and antimicrobial volatile organic compounds (VOC’s) [18,32, 33] See Table 2.

2.1 An Engineering approach to bioprocess development and design for biopreservatives and post-harvest control: A focus on control agents from yeasts

In bio-systems engineering, microorganisms utilise nutrients for their physiological activities; in doing so, cellular proliferation occurs, leading to the accumulation of intra and/or extracellular products [34]. Generally, primary and secondary metabolites are produced during different fermentation stages. Amino acids, lipids, carbohydrates, nucleic acids and proteins are produced as primary metabolites during cellular growth, while secondary metabolites such as penicillin, cephalosporin, ergotrate and statins are also produced after the exponential growth phase [35]. Process engineering principles are governed by the understanding and elucidation of parameters involved in any production system. In bioprocess engineering systems for example, it is vital to identify, explain and optimise production in order to mitigate input cost and to be able to get the needed operational guidelines of the process. In fermentation technology, key parameters such as substrate requirements and concentration, pH, temperature, salinity and nitrogen source ratio, including disolved oxygen requirements, must be optimised in order to guarantee optimal cell density and extracellular compound production [36,37]. For optimal production conditions, the development of models describing process kinetics is essential and, also facilitates statistical analyses and process optimisation. Additionally, the engineering aspect of a biological system can also assist in developing processes with low input costs for downstream processes, albeit achieving a high yield of the products of interest.


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Tab

le 1

Exa

mpl

es o

f an

tim

icro

bial

com

poun

d pr

oduc

ing

yeas

ts [

11,1

6,38

-40]

.

Yea

st sp

ecie

s A

ntim

icro

bial

com

poun

d id

entit

y, m

olec

ular

siz

e, te

mpe

ratu

re a

nd/o

r pH

act

ivity

A

pplic

atio

n M

echa

nism

of a

ctio

n Ta

rget

yea

st

Cand

ida

(form

erly

nam

ed

Toru

lops

is gl

abra

ta)

n/d

n/d

Dam

ages

the

plas

ma

mem

bran

e Sa

ccha

rom

yces

ce

revi

siae

Ca

ndid

a py

ralid

ae

CpK

T1

and

CpK

T2

(>50

KD

a); p

H: 3

.5 –

4.5

; te

mpe

ratu

re: 1

5 an

d 25

ºC

G

rape

juic

e n/

d Br

etta

nom

yces

br

uxel

lens

is Kl

uyve

rom

yces

wi

cker

ham

ii K

wkt

(72

kDa)

; pH

: 3.8

-4.6

; tem

pera

ture

: 25

ºC

Win

e m

akin

g β-

1,6-

gluc

ans

rece

ptor

Br

etta

nom

yces

. br

uxel

lens

is Te

trapi

sispo

ra p

haffi

i K

pkt (

33 k

Da)

; pH

: 3 -

5; t

empe

ratu

re: <

40 º

C

Win

e m

akin

g D

isru

pts

the

inte

grity

of

the

cell

wal

l. A

lso

show

s β-

gluc

anas

e ac

tivity

H. u

varu

m

Will

iops

is m

raki

i NC

YC

50

0 K

-500

(1.

8-5.

0kD

a); p

H: 2

.4 –

4.0

te

mpe

ratu

re :

30 º

C

Ant

ifun

gal a

gent

M

embr

ane

perm

eabi

lity

Cand

ida

albi

cans

and

Sp

orot

hrix

sche

nkii

Pich

ia

Acac

ia (r

ecla

ssifi

ed a

s M

iller

ozym

a ac

acia

e)

PaT

(18

7 kD

a); p

H:7

– 7

.5 a

nd 5

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6.6

te

mpe

ratu

re :

n/d

n/d

Cel

l cyc

le a

rres

t in

G1

phas

e in

S.

cer

evis

iae

cell

s. D

ispl

ays

chiti

nase

act

ivity

S. c

erev

isia

e

Han

seni

aspo

ra u

varu

m

18 k

Da;

pH

: 3.7

– 3

.9

tem

pera

ture

: n/

d n/

d β-

1,6-

gluc

ans

rece

ptor

C.

alb

ican

s, Sp

orot

hrix

sp

., Sc

henk

ii sp

., H

eter

obas

idiu

m sp

., Po

stia

sp.,

Serp

ula

sp.

and

Fusa

rium

sp.

Pich

ia a

nom

ala

DB

VPG

30

03

Pik

t (8

kDa)

; pH

: 4.4

; tem

pera

ture

: 25

– 3

5 °C

W

ine

mak

ing

β-1,

6-gl

ucan

s re

cept

or

B. b

ruxe

llens

is

n/d-

not d

eter

min

ed


221

_____________________________________________________________________________

Table 2 Examples of potential biocontrol yeasts assessed against fungal pathogens in post-harvest spoilage control of fruits [32,41-45].

Fruit Fungal pathogen Biocontrol yeasts Apple Botrytis cinerea Candida saitoana Apple Penicillium

expansum Candida guilliermondii, and Saccharomyces cerevisiae M25

Apple Penicillium expansum Botrytis cinerea

Rhodotorula mucilaginosa

Apple Botrytis cinerea Pichia guilliermondii Grapes Botrytis cinerea Saccharomyces cerevisiae and Schizosaccharomyces pombe Grapes Botrytis cinerea Candida sake CPA-1 and Fungicover Pears Penicillium

expansum Botrytis cinerea

Cryptoccocus albidus NPCC 1248, Pichia membranifaciens NPCC 1250, Cryptoccocus victoriae NPCC 1263, NPCC 1259

The effect of temperature on the growth and stability of extracellular biopreservation compounds has been studied [46]. In the study by Robledo-Leal et al. [46], biopreservative behaviour within the C. parapsilosis complex and the biopreservative activity of C. metapsilosis strains occurred at 25 °C. The temperature at which the process was carried out was crucial for the biopreservation compound production and the optimum biopreservation efficacy temperature was reported between 15–20 °C. The effect of temperature on the stability of the biopreservation compound revealed that it was still active at temperatures above 30 °C. A different study showed that, temperature and pH played a significant role on the production and stability of the biopreservation compounds from a Candida pyralidae strain [47]. The authors also highlighted the importance of pH and temperature on the biopreservation compound production in a single stage bioreactor, and optimal production conditions in that study were at pH 5 and 22.5ºC. In order to fully understand the fermentation parameters involved in such biological systems, the said examples (pH and temperature) are critical for designing appropriate bioprocess systems. Although selected parameters can be optimised, industrial scale process optimisation still remains a challenge, especially during antimicrobial compound production from yeasts. However, the knowledge associated with the growth limiting substrate, the ratio of carbon to nitrogen (C: N) in the medium are among other parameters that can be considered for process scale-up. To date, synthetic refined media are used for biopreservation compounds production studies. However, the use of such refined media in the biopreservation compounds production is seldom recommended due to high cost. For optimal and sustainable production of biopreservation compounds, the following critical questions must be fully addressed. 1) What other suitable, high yield and cost effective substrates can be used for production? 2) Can other media or substrates be used and optimised for production under optimum bioreactor conditions? 3) Bioreaction vessels such as flasks are commonly used for production of antimicrobial compounds, what is the most suitable bioreactor system for achieving optimal yield?

2.2 Bioreactor operation and selection

Regardless of whether the product is a primary or a secondary metabolite, a need exist to develop a better system for producing safer and cost effective biopreservatives. Recently, a single stage bioreactor was used to produce antimicrobial compounds, from a yeast i.e. Candida pyralidae KU736785 [47]. The authors reported maximum biopreservation compound production during exponential growth phase. This study also shwohed that the produced biopresevation compound was a primary metabolite, but further downstream processing remained a challenge, particularly during supernatant recovery stages. Maintaining a high cell density in the exponential growth phase is important and using membrane bioreactor (MBR) technology presents key advantages for the collection of cell free supernatant, and for continuous product recovery. The choice of a reactors’ operational mode is important in the modelling and design of the process to be used. Furthermore, the aim of effective bioreactor design is the ability to control key variables, to contain and positively affect the process. For bench-scale experiments, batch, semi-batch and continuous systems are used and each of these processes present advantages and disadvantages. For instance, cell recycling in continuous cultures can be used at steady-state with a continuous feed. The system is capable of elevating productivity, while lowering labour intensivity, but negatively reducing product concentrations. Nevertheless, these processes and parameters can be optimised to achieve maximum yields using statistical design optimisation methods, such as response surface methodology (RSM), with a central composite design (CCD) [48-50].


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3. Commercially produced biopreservatives and biocontrol agents

Biopreservatives are not produced nor used on a large scale due to inadequacy of process engineering systems used in their production and application in fast-moving consumer goods (FMCG) or consumer packaged goods (CPG). Many researchers have reported that some partially identified compounds could be used in food, beverage and fruits preservation but that, the use of microorganisms as producers of safe preservation compounds has not been fully applied [11,16,17,51]. Examples of biocontrol agents acting against post-harvest pathogens that are currently commercialised are based on either one or two strains of yeasts. For example, Shemer TM (AgroGreen, Asgdod), is a biofungicide formulated using Metschnikovia fructicola. CandifruitTM (SIPCAM INAGRA, S.A., Valencia, Spain) using Candida sake for pome fruits. Boni-ProtectTM (Bio-ferm, Germany) is produced from two strains of Aureobasidium pullulans. Due to uncertainties related to the use of some yeasts in post-harvest spoilage control against spoilage organisms, what of the compounds that they produce? Could they be used in the same manner or could they be applied elsewhere to extend their applications? Can there be yeasts capable of acting as both post-harvest control agents and producers of biopreservation compounds with broader antimicrobial activity thus appeal to the FMCG and CPG industry? These questions must be a focus of the ongoing research effort to mitigate the associated risks of synthetic chemical preservatives.

4. Biopreservatives and post-harvest biocontrol using Candida pyralidae KU736785 as a model study

4.1 Growth/production kinetics, subsequent to process modelling and optimisation

Current research clearly demonstrates the potential that yeasts have as either biocontrol agents and/or producers of antimicrobial compounds. Although few compounds of different characteristics have been identified, many of these compounds are not produced and used at an industrial scale. This could be attributed to production process design and optimisation deficiencies. In a study by Mewa-Ngongang et al. [47], kinetic modelling and optimisation of biopreservation compound production was assessed using Candida pyralidae KU736785, with preliminary screening against fungal pathogen, Botrytis cinerea and beverage spoilage organism, Candida guilliermondii. The in-vivo test was conducted using disinfected apples in which apples were wounded (3 mm deep and 2 mm wide) along the center, with each wound being inoculated with 15 µL of Candida pyralidae at a concentration of 1 x 108

cells.mL-1, subsequent to the addition of a spore suspension of the spoilage fungus (B. cinerea) at 105 conidia/mL. The apples were then incubated at 25 ºC for seven days. The ability of Candida pyralidae to minimise post-harvest decay on the apple was used as a positive result. For fractionation, different fractions tested were obtained from a size exclusion chromatographic (SEC) system. An isocratic elution with 5 mM sodium citrate at pH 4.5 over 2 column volumes at a flow rate of 1 mL.min-1, was used and 25 fractions were obtained. The resin used was Toyopearl HW-55F. All 25 fractions were first tested against Candida guilliermondii. Fractions that showed growth inhibiton activity against Candida guilliermondii were tested in-vivo against Botrytis cinerea. The test was conducted as discribed above with the diffrence that 15 µL of the SEC fraction was administered in the wound in replacement of 15 uL of the Candida pyralidae broth. The in-vivo efficacy test of C. pyralidae KU736785 against B. cinerea on apple showed that C. pyralidae KU736785 completely reduced the disease incidence (DI) (100% DI reduction). Disease incidence was determined by comparing the lesion diameter (LD 27.38 mm) of the negative control with that of the tested samples. This showed that C. pyralidae KU736785 was able to minimise decay caused by B. cinerea under commercial storage conditions (Fig 1). Fractions A8 to A12 showed growth inhibition activity against Candida guilliermondii on the plate assay (Fig. 2a). However, fractions A9 and A12 were also able to considerably reduce the decay caused by B. cinerea on apples (Fig. 2b). The results obtained suggested that a purified crude biopreservative sample from a fermentation broth innoculated with C. pyralidae KU736785 under optimum pH and temperature can have a broader spectrum of biopreservation activity, as shown in Fig. 2 with B.cinerea inhibition (A9 and A12). These findings suggested that there could be more value to produce biopreservatives from a single yeast strain that shows growth inhibition activity against atleast one spoilage organism. If the biopreservation activity is also based on the concentration of the antimicrobial compounds present in fermentation broth, an engineering approach to biosystem design and optimisation for production is thus inevitable.


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Fig. 1 Post-harvest control activity of Candida pyralidae KU736785 in controlling spoilage caused by Botrytis cinerea, on Malus domestica.

a b

Fig. 2 (a) = Size exclusion chromatography fractions A8, A9, A10, A11 and A12 tested against Candida guilliermondii [47]; (b) = Post-harvest control activity against Botrytis cinerea, on Malus domestica; using compounds produced by Candida pyralidae KU736785.

4.2 Redefining the zone of inhibition/clearance

The screening, production kinetics and optimisation of the growth inhibition compound by C. pyralidae KU736785 was investigated. The growth inhibition assay during the screening and the testing of the crude sample from the fermentation was conducted as described by [47]. During the production kinetic study and optimisation, it was imperative to quantify the production of the compound at different times and under different conditions of the bioprocess used. Generally, there has been a limited approach in quantifying the effect of biopreservation compounds against spoilage organisms. It

Negative control

C. pyralidae KU736785

Negative control

A8

A10

A9

A12

A11


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was therefore important to find a new approach for biopreservation compound activity quantification for application in bioprocess development, which led to the conceptualisation of the volumetric zone of inhibition (Fig. 3).

Fig. 3 Schematic outline of the volumetric zone of inhibition concept that results from injecting a volume of 20 µL of the crude sample of the antimicrobial compound into a solidified media seeded with a spoilage organism at a concentration of 106 cells.mL-1 [47]. Whereby: H (similar to height of a cylinder) is the thickness (0.2 cm), A represents the circular zone of inhibition quantified as surface area (cm2) which includes the pierced well where the biopreservation compound is spotted, d (cm) is the diameter of the pierced well, D0 (cm), from which d is substracted, corresponds to the total zone of inhibition. D (cm) is then the resulting diameter corresponding to the diameter zone of inhibition generated by the volume (0.02 mL) of the cell free biopreservation compounds introduced into the pierced well. With the aforementioned parameters, the volumetric zone of inhibition can then be estimated using Equation 1, i.e. Area of the circular surface of inhibition (A) x thickness (H) of the contaminated solidified media. (r =D/2); . (1) The interpretation of the volumetric zone of inhibition (VZI) is such that a volume of the crude antimicrobial sample is sufficient to inhibit the growth of the spoilage organism at a known concentration. This means a homogeneous quantity of food or beverage that a known volume of the biopreservation compound could preserve. By using this method, inhibition can be quantified as a litre of contaminated solidified media (L CSM) per mL of antimicrobial compound used (mL ACU) denoted using units L CSM/mL ACU [47]. Furthermore,when studying the production kinetics of biopreservation compounds production from microorganisms during a fermention, the rate of biopreservation compound production could also be quantified using this approach. The inhibition activity rate for assessment of process kinetics could in turn be described as the volumetric zone of inhibition that a specific volume of the antimicrobial sample would yield at a specific time during fermentation, denoted by L VZI.mL-1 ACU.h-1. Many studies have reported on antimicrobial compounds originating from various sources, i.e. plant extracts and microorganisms [16,52]. However, for effective application, the antimicrobial activity should be quantified in a manner suitable for use in mathematical models. Due to these limitations, the following questions can further be used to thouroughly understand model development for bioprocess development at an industrial scale. How effective will this concept be useful in biosystem design for biopreservative production at an industrial scale? What will other inhibitory indeces be, to efficiently describe fermentations for biopreservation compound production as well as the biopreservation activity quantification? As far as media selection/optimisation is concerned, most research currently conducted on antimicrobial/biopreservation compounds use growth medium such as yeast peptone dextrose (YPD), which is


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inapplicable on an industrial scale. Currently, there is minimal indication in exploring medium design for industrial biopreservation compound production.

5. Conclusion

Continues food, fruits and beverages losses are experienced at a large scale in industry. The current control methods present many challenges such as health related concerns, while consumers demand natural and safer preservatives. Despites these challenges, the current use of synthetic chemicals as preservatives have not addressed the issue of food losses caused by microbial spoilage. Besides, spoilage organisms have also developed resistance to some of the chemical preservatives. Yeasts have been found to be a potential alternative to chemical preservatives. However, the findings are still superficial in addressing the current need for safer and cost effective preservatives. In this regard, it is demonstrated that an appropriate production system using an engineering approach could advance the development and the use of yeasts, including their extracellular compounds as fruit biocontrol agents and as biopreservatives. The following points could be at the centre of future studies in biopreservation compounds production: 1) The carbon and nitrogen renewable sources that can be explored for the design of an industrial fermentation medium for biopreservatives production. 2) Design of an apropriate fermentation system and models for the optimum biopreservation compounds production, provided that a suitable fermentation medium is developped. 3) Development of suitable method for biopreservation compounds activity quantification to assess and validate the production system and the efficacy of the biopreservation compounds produced.

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