CHAPTER ELEVEN

Modification of the ColonicMicrobiotaJuliet Ansell*,1, Shanthi Parkar†, Gunaranjan Paturi‡,Douglas Rosendale*, Paul Blatchford**The New Zealand Institute for Plant & Food Research Limited, Private Bag 11600, Palmerston North,New Zealand†The New Zealand Institute for Plant & Food Research Limited, Private Bag 3123, Hamilton, New Zealand‡The New Zealand Institute for Plant & Food Research Limited, Private Bag 92169, Auckland, New Zealand1Corresponding author: e-mail address: juliet.ansell@plantandfood.co.nz

Contents

1.

AdvISShttp

Introduction

ances in Food and Nutrition Research, Volume 68 # 2013 Elsevier Inc.N 1043-4526 All rights reserved.://dx.doi.org/10.1016/B978-0-12-394294-4.00011-0

205

2. Modification of the Colonic Microbiota by Kiwifruit Polyphenolic Compounds 206 3. Modification of the Colonic Microbiota by Kiwifruit Carbohydrates 207 4. Kiwifruit Fermentation Offers Functional Benefits to the Gut 215 5. Conclusion 215 References 216

Abstract

It is becoming clear that the ecology and functionality of the human gut microbiota areextremely diverse and complex. The microbiota have coevolved with us metabolicallyto live symbiotically and to share the workload of extracting nutrients and energy fromthe diet. It is also clear that a diet rich in fruit, vegetables, and whole grain cereals is goodfor general health and gut health and that this is due partly to the phytochemicals andpartly to the nondigestible carbohydrates (or dietary fiber) that are present in plants.Kiwifruit contain polyphenolics and nondigestible carbohydrates in the form of pectic,hemicellulosic, and cellulosic polysaccharides, all of which can be degraded by variousmembers of the gut microbiota and result in beneficial effects. This chapter summarizeshow kiwifruit act tomodify the colonic microbiota and the resultant beneficial effects onhuman health.

1. INTRODUCTION

A healthy balance of bacteria colonizing the adult gastrointestinal tract

is essential for the breakdown and metabolism of foods as well as for the pro-

duction of microbially synthesized vitamins. From a health perspective, the

205

206 Juliet Ansell et al.

gut microbes play a crucial role in the competitive inhibition of pathogens

and enhanced immunity through secretory and excretory substances that in-

teract with other microbes and the gut lining. Conversely, diet can have a

profound influence on the composition of the microbiota in the adult gut

(Macfarlane, Bahrami, & Macfarlane, 2011). What we eat can modulate

the colonic flora directly and influence resulting gut health.

The modern diet is said to be energy rich but nutrient poor with many

foods comprising “empty calories” rather than healthful nutrients. Although

there is still some debate around the definition of a nutrient-dense food,

fruits and kiwifruit in particular are accepted as being naturally nutrient rich

(Drewnowski, 2005), containing vitamin C, carotenoids, polyphenols,

flavonoids, fiber, folate, and zinc. Some of these nutrients are absorbed in

the upper gastrointestinal tract, as described elsewhere in this volume, but

others pass through to the colon and interact with the microbiota that reside

there. Polyphenols, mainly procyanidins and flavonol glycosides (Dawes &

Keene, 1999), as well as fiber fractions such as pectic polysaccharides rich in

arabinose, galactose, and galactose (Dawson & Melton, 1991), have been

characterized in green and gold kiwifruit and these are likely to transit to

the large intestine intact. Once in the large intestine, there are several ways

in which components of kiwifruit may modulate the colonic microbiota:

– Polyphenolics reaching the colon may directly stimulate the growth of

beneficial bacteria or act as antimicrobial agents against pathogens.

– Nondigestible polysaccharides fermented by the microbiota may induce

selective growth of beneficial bacteria.

The modulation of microbial growth is just the start of a cascade of events, as

microbial growth is associated with an increase in microbial metabolism,

which in turn releasesmoremetabolites into the gut environment.Highermi-

crobial growth may also translate to a higher turnover of bacteria, with some

breakdown products of lysis (bacterial cell wall fragments or DNA) potentially

also having an impact on the gut environment and mucosal immunity.

2. MODIFICATION OF THE COLONIC MICROBIOTABY KIWIFRUIT POLYPHENOLIC COMPOUNDS

Promotion of a healthy colonic environment is partly about selectively

enhancing the growth of beneficial bacteria but also involves the competitive

inhibition of potentially pathogenic bacteria. Both green (Actinidia deliciosa

‘Hayward’) and gold (A. chinensis ‘Hort 16A’) kiwifruit extracts have demon-

strable antimicrobial activity against potential gut pathogens while increasing

207Modification of the Colonic Microbiota

the growth of lactic acid bacteria. Aqueous extracts of the edible portion

inhibited monocultures of Staphylococcus aureus, Streptococcus mutans, Salmonella

enterica serovarTyphimurium, andEscherichia coli, whereas growth of lactic acid

bacteria Lactobacillus rhamnosus, Lactobacillus acidophilus, and Bifidobacterium breve

were increased (Molan, Kruger, De, & Drummond, 2007).

Similarly, using a fluorescent bacteria adhesion assay,wehave examined the

abilityof total kiwifruit polyphenolextracts toprevent theadhesionofS. enterica

(serovar Typhimurium; Parkar et al., 2010), by incubating antibiotic-free

14-dayCaco-2cell cultureswithpolyphenol extractsobtained fromtheaqueous

phase of green and gold kiwifruit (Hunter, Greenwood, Zhang, &

Skinner, 2011) at concentrations of 50 mg/mL for 1 h. This resulted in

a modest decrease in the adhesion of S. enterica (serovar Typhimurium)

to Caco-2 cells (14% and 9% respectively; S.G. Parkar, unpublished data).

Green kiwifruit contain the polyphenolics caffeic acid, catechin, chlo-

rogenic acid, epicatechin, p-coumaric acid, and quercetin derivates (Dawes &

Keene, 1999; Latocha, Krupa, Wolosiak, Worobiej, & Wilczak, 2010;

Sun-Waterhouse et al., 2009), and as described in Chapter 6. Commercial

preparations of these polyphenols have also been shown to generate a

dose-dependent decrease in S. enterica (serovar Typhimurium) adhesion to

Caco-2 cells (Parkar, Stevenson, & Skinner, 2008), thereby indicating a likely

role of these compounds in the previously observed inhibition by kiwifruit.

While relative to other fruit, kiwifruit are not particularly rich in total

phenolics (Hunter et al., 2011), they are rich in vitamin C. To explore

interactions between kiwifruit polyphenols and vitamin C against Salmonella

adhesion, quercetin was chosen as a representative kiwifruit polyphenol

(Dawes & Keene, 1999). As shown in Fig. 11.1, vitamin C was found to

inhibit the adhesion of S. enterica (serovar Typhimurium to Caco-2) cells

at concentrations of up to 62.5 mM. However, in the presence of 40 mMquercetin, vitamin C was protective even at 31.25 mM. Thus, polyphenols

and vitamin C may combine to generate synergistic inhibitory effects on the

adhesion of pathogenic bacteria to the gut wall.

3. MODIFICATION OF THE COLONIC MICROBIOTABY KIWIFRUIT CARBOHYDRATES

Kiwifruit carbohydrates that escape digestion may act as prebiotics.

A prebiotic is defined as a food ingredient that is not hydrolyzed by the

human digestive enzymes in the upper gastrointestinal tract and beneficially

Vitamin C (mM)

Vitamin C

% A

dhes

ion

of S

.ent

eric

a sv

Typ

him

uriu

m

Vitamin C + 40 mM quercetin

20

0

40

60

250

*

125 62.5 31.1

80

100

120

Figure 11.1 Effect of vitamin C and quercetin on adhesion of Salmonella enterica(serovar Typhimurium) to Caco-2 cells. The cells were pretreated with vitamin C at halfdilutions from 250 mM, with or without 40 mM quercetin, and then incubated with fluo-rescent bacteria for a further 2 h. The percentage of adherent bacteria was calculatedafter washing the cells free of loosely unattached bacteria. The values are % adhesion offluorescent bacteria �SEM. The asterisk denotes significance at P<0.05, in comparisonwith the control, which was normalized to 100%.

208 Juliet Ansell et al.

affects the host by selectively stimulating the growth and/or activity of one

or a limited number of bacterial species in the colon (Gibson, Probert, Loo,

Rastall, & Roberfroid, 2004). The true impact of prebiotic fiber may be

through the modulation of gut microbiota to generate organic acid meta-

bolites that are valuable to the host, and that support a healthy population

of microbiota in the colon. The major organic acids generated include for-

mate, lactate, succinate, short-chain fatty acids such as acetate, propionate,

and butyrate, and branched acids such as isobutyrate. These acids are ben-

eficial for the host and are rapidly absorbed in the colon for energy

(ATP) production (butyrate), lipogenesis (acetate), and gluconeogenesis

(propionate) (Hijova & Chmelarova, 2007). These acids, and specifically

butyrate, have been found to be essential in stimulating growth of intestinal

mucosal cells in mice (Kripke, Fox, Berman, Settle, & Rombeau, 1989).

While growth of beneficial microbes may act to out-compete potential

pathogens, the acids they produce may also inhibit gut pathogens. For

example, lactate and acetate are known to inhibit the growth of Gram-

negative pathogens such as E. coli (Makras & De Vuyst, 2006) and even

prevent their translocation across the gut lumen (Fukuda et al., 2011).

209Modification of the Colonic Microbiota

Kiwifruit contain about 2–3% cell wall nonstarch polysaccharides

(NSPs), comprising soluble pectic polysaccharides (homogalacturonans and

rhamnogalacturonans substituted with galactan and arabinogalactan side

chains), insoluble trifluoroacetate–soluble hemicellulosic polysaccharides

(xyloglucan, glucuronoarabinoxylan, and galacto-(gluco)-mannan), and insolu-

ble trifluoroacetate–insoluble cellulose (Carnachan,Bootten,Mishra,Monro,&

Sims, 2012). These are described in more detail in Chapter 5. The chemical

composition and structure of these NSPs remain largely unchanged after

digestion, albeit with a decrease in the degree of methyl esterification of

galacturonic acid residues (Carnachan et al., 2012); so they pass intact to the large

intestine, where they become substrates for microbial fermentation by the resi-

dent microbiota, and can serve to enrich fractions of the microbiota known to

confer probiotic benefits on the host. As an example, pectinwith a lowdegree of

polymerization has been shown to promote butyrate production while pectin

with a high degree of polymerization promotes propionate production

(Nilsson &Nyman, 2005). Thus, the quality and quantity of fiber released after

digestion may play a major role in determining its prebiotic potential.

The ability of the gut microbiota to catabolize carbohydrates and gener-

ate organic acids and other fermentation by-products has been the subject of

review (Louis, Scott, Duncan, & Flint, 2007). A subsequent review covers

the mechanism of carbohydrate utilization in more detail (Flint, Bayer,

Rincon, Lamed, & White, 2008). Essentially, the ability of members of

the microbiota to utilize kiwifruit carbohydrates for energy is dictated by

their arsenal of degradative enzymes (glycoside hydrolases, polysaccharide

lyases, and carbohydrate esterases), adhesion factors, and transport systems

for each substrate (Flint et al., 2008). This results in an array of

carbohydrate-degrading mechanisms employed by so-called primary feeders

(those members of the microbiota able to ferment the substrate directly) and

subsequent secondary feeders that make use of released oligosaccharides or

fermentation by-products from the primary feeders.

Twowell-studied systemsexemplifyextremeparadigmsofcarbohydrateus-

age employed bymembers of the gut microbiota: the extracellular cellulosome

paradigm exemplified by members of the Gram-positive Ruminococcus genus,

whichwould be required for the degradation of insoluble kiwifruit xyloglucan,

glucuronoarabinoxylan, galacto-(gluco)-mannan and cellulose, and the largely

cell-associated sequestration paradigm exemplified by the Gram-negative

Bacteroides thetaiotaomicron, which would be required for the utilization of

soluble kiwifruit homogalacturonans and rhamnogalacturonans.

210 Juliet Ansell et al.

The Gram-positive, extracellular system features a multienzyme com-

plex tethered to a structural protein scaffold. This complex may incorporate

a binding module, glycosidases, and elements to modulate the number of

components comprising the cellulosome. Oligosaccharides released from

the hemicellulosic and cellulosic polysaccharides by the cellulosomal degra-

dation are taken up by transporters on the single cell membrane of the Gram-

positive bacterium. By-products expected from this fermentation include

hydrogen, carbon dioxide, and the organic acids formate, acetate, and suc-

cinate. Solubilized carbohydrates thus produced can act as a nutrient source

for Bacteroides (which in turn generate fermentation products, also including

propionate) and clostridial members of the Firmicutes genus such as Roseburia

spp. and Butyrivibrio, while the fermentation by-products themselves benefit

methanogens, acetogens, and the clostridial members. This latter group, in

turn, generates butyrate in addition to hydrogen, carbon dioxide, formate,

and acetate.

The Gram-negative, cell-associated system features “starch utilization”

(Sus) binding molecules on the outer membrane of the Bacteroides genera

which bind the pectic polysaccharide molecules to the cell surface, where-

upon the action of degradative enzymes releases and exposes oligosaccharides

to further degradation by additional glycosidases as they transit the periplasm,

cytoplasmic membrane and, via transporters, the cytoplasm. Waste products

include hydrogen, carbon dioxide, formate, acetate (which acts as a nutrient

for later members of the food chain), succinate, and propionate.

Structural differences in the responsible bacteria (single envelope vs.

double envelope enclosing the periplasmic space) and differences in the

physicochemistry of their preferred substrates (insoluble or soluble)maydictate

these different (extracellular breakdown vs. sequestration) approaches to kiwi-

fruit carbohydrate utilization. However, for both the systems described above,

successful carbohydrate-degrading bacteria possess multiple redundancies in

their degradative arsenals, as the loss of an “only-copy” would be catastrophic

to the survival of their possessors. Further, the glycosidase component of these

degradative systems shows considerable similarity in primary sequence, struc-

tural topology, and catalytic behavior across all bacteria. This enables the activ-

itiesof these enzymes tobedetermined in simple assay systems, such as theuseof

colorimetric enzyme substrates (Riley & Wertz, 2002).

A recent attempt to quantify some of these processes involved in kiwi-

fruit degradation used an in vitro batch fermentation system, minimizing the

confounding influence of host carbohydrates. Fresh whole green kiwifruit

were subjected to simulated gastric-small intestinal digestion, thus simulating

211Modification of the Colonic Microbiota

the physicochemical modifications that kiwifruit undergo as they transit

through the upper gut. The large polysaccharides remaining after dialysis

of the kiwifruit digesta were fermented for 48 h with fecal slurries obtained

from healthy donors. By assessing changes in the abundance of key microbial

phyla and determining glycosidase activities and fermentation by-product

(organic acid) generation, the degradation of kiwifruit polysaccharide by

the complex food web of the microbiota was investigated.

Real-time quantitative PCR was used to demonstrate that both gold

and green kiwifruit altered specific human microbial populations

over 48 h. Both kiwifruit substrates increased the total bacteria, Bacte-

roides–Prevotella–Porphyromonas group, Lactobacillus, and Bifidobacterium spp.

compared with the control (Parkar et al., 2012). Similar increases in bacterial

populations were reported by Han, Balan, Molist Gasa, and Boland (2011),

where a higher abundance of total bacteria and members of the Bacteroides

group, and an increase in the ratio of Lactobacillus to Enterobacteria were

observed in the colon of growing pigs fed green kiwifruit fiber compared

with those fed a control diet.

These prebiotic effects have since been explored in greater detail, using

16S rRNA pyrosequencing (Fig. 11.2) of the microbial DNA prepared from

the green kiwifruit fermenta from that same study (Parkar et al., 2012). Batch

fermentation with green kiwifruit led to an immediate and lasting reduction

in the average percentage abundance of all members of the Proteobacteria

phyla; Bacillaceae and Clostridiaceae members of the Firmicutes phyla; and

Prevotellaceae from the Bacteroidetes phyla, which were present in the original

fecal inocula from 10 donors. The abundance of Ruminococcaceae (Firmicutes)

was halved after 24 h. In contrast, Bacteroidaceae, Lachnospiraceae, and

Veillonella members of the Firmicutes phyla and Coriobacteriaceae of the

Actinobacteria phyla increased relatively following 24 h of exposure to green

kiwifruit. The increases in Lachnospiraceae remained sustainable after 48 h.

Coriobacteriaceae continued to increase relatively, accompanied by increases

in Bifidobacteraceae (Actinobacteria) together with a slight resurgence in

Ruminococcaceae and Enterobacteraceae (Proteobacteria). After 48 h, the increased

levels of other bacteria observed at 24 h were not sustainable and had

decreased in relative abundance. These changes appeared to correlate

with the expected roles and carbohydrate utilization capabilities of the

various members of the gut microbiota. Known dietary carbohydrate uti-

lizers such as Lachnospiraceae and Bacteroidaceae were able to make early use

of the kiwifruit substrate, particularly soluble pectic homogalacturonans

and rhamnogalacturonans, and of the insoluble hemicellulosic xyloglucans,

Rikenellaceae

Prevotellaceae

Porphyromonadaceae

Bacteroidaceae

Veillonellaceae

Streptococcaceae

Ruminococcaceae

Lachnospiraceae

Erysipelotrichaceae

Enterococcaceae

Clostridiaceae

Bacillaceae

Coriobacteriaceae

Bifidobacteriaceae

Rhodospirillaceae

Moraxellaceae

Enterobacteriaceae

Burkholderiaceae

AlcaligenaceaeP

rote

obac

teria

Act

inob

acte

riaF

irmic

utes

Bac

tero

idet

es

00

60

Mic

robi

al a

bund

ance

120

180

24 48

Time (h)

Figure 11.2 The changing fecal microbial abundance over time during in vitro batchfermentation of green kiwifruit digesta using fecal inocula from 10 separate donors,as determined by 16S rRNA pyrosequencing. Microbial abundances were calculatedas themean of the percentage sequence abundance from each of the 10 donors at eachtime point, and have not been scaled to the sum of taxa percentages within time periods,but remain comparable at the taxa level across the time points. The greater abundance atthe 0-h time period reflects the greater number of taxa observed across the donors.Sequences of less than 1.0% abundance were excluded from the analysis. The four mostabundant phyla are shown: Bacteroidetes (Red), Firmicutes (Green), Actinobacteria (Blue),and Proteobacteria (Orange). Taxa at the family level are depicted by different shadesof the phylum color as shown in the legend.

212 Juliet Ansell et al.

glucuronoarabinoxylans, and galacto-(gluco)-mannans liberated from the

kiwifruit but not necessarily utilized by the cellulose-degrading members

of the microbiota (Carnachan et al., 2012; Flint et al., 2008). In contrast,

members of the gut microbiota that were either poorly optimized to

213Modification of the Colonic Microbiota

compete for dietary carbohydrate in a closed system (Proteobacteria), or

known to exhibit a preference for host (mucin) carbohydrate

(Prevotellaceae and, to some extent, Ruminococcaceae), declined relative to

the more numerous bacteria. After 48 h, it is expected that only the most

robust or specialized primary carbohydrate degraders would be able to make

use of remaining, poorly accessible kiwifruit sugar residues, such as poorly

fermented or underutilized cellulosic carbohydrates. This may explain the

observed resurgence of Ruminococcaceae, which possess the extracellular

cellusomal degradative system discussed above. Those degraders with a

cell-associated soluble carbohydrate-utilizing system, such asBacteroidaceae de-

clined in numbers relative to the more abundant or increasing Firmicutes and

Actinobacteria. It is likely that secondary metabolizers such as Bifidobacteriaceae

and perhaps Enterobacteraceae could continue to make use of metabolic

by-products and also obtain nutrients from dying bacteria.

These microbial data correspond with the glycosidase activities recorded

from these fermenta (Table 11.1 and Parkar et al., 2012). Statistically

significant increases in activity were observed with almost all substrates

(fucose, galactose, glucose, uronic acid, arabinose, rhamnose, and xylose)

used. The corresponding sugar residues comprise the pectic andhemicellulosic

fractions of the kiwifruit (Carnachan et al., 2012); these are the substrates the

abundantBacteroidaceae andLachnospiraceae are expected to utilize or, in the case

of hemicellulosic sugars, theRuminococcaceae to release for utilization by others.

For example, a decrease inmannosidasewas noted to correspond to a rapid de-

cline inavailablemannoseof yeastorigin in the fermentationmedia, reinforcing

that the changes in activities observed tended to correspond to microbial car-

bohydrate utilization over time.

The microbial fermentation by-products (namely the organic acids ace-

tate, propionate, and butyrate) were observed to increase in the presence of

kiwifruit fermenta, while lactate and succinate concentrations declined after

24 h, lactate remained low at 48 h, and succinate increased (Table 11.1 and

Parkar et al., 2012). A decline in lactate and succinate would be expected in a

batch fermentation. They may act as metabolic intermediates or cross-

feeding substrates for the further generation of acetate and propionate,

respectively. Most of the genera observed by pyrosequencing are acetate

producers. Propionate is a product of Bacteroidetes fermentation, and also

produced by Veillonella and other members of the Firmicutes phyla. Butyrate

is produced by members of the Firmicutes subset which features members of

the Lachnospiraceae family, among others (Louis et al., 2007). While it would

be an oversimplification to state that these acids specifically correlate with

those taxa observed to increase with kiwifruit fermentation, all acid

Table 11.1 Percentage change in organic acid concentrations and glycosidase activitiesafter 24 and 48 h of fermentation of green kiwifruit using a human fecal inoculum,relative to 0 h controlTime (h) 24 48

Organic acid concentration (% concentration relative to 0 h)

Acetate 449.8 555.5

Propionate 700.9 1022.3

Butyrate 1179.1 1940.9

Formate 288.1 37.2

Lactate 62.4 40.8

Succinate 11.6 819.2

Glycosidase activity (% activity relative to 0 h)

a-Fucosidase 252.4 255.4

a-Galactosidase 181.9 159.2

b-Galactosidase 169.7 129.3

a-Glucosidase 262.5 215.3

b-Glucosidase 267.8 227.6

b-Glucuronidase 200.4 204.5

a-Mannosidase 43.2 31.6

a-Arabinofuranosidase 175.1 168.8

a-Rhamnosidase 236.5 213.5

b-Xylosidase 268.3 235.3

Data adapted from Parkar et al. (2012)

214 Juliet Ansell et al.

concentrations are explainable in the context of changes in fecal microbiota

upon kiwifruit fermentation.

Collectively, these microbial numbers, microbial abundance data, glyco-

sidase activities, and organic acid by-product concentrations show that con-

sumption of kiwifruit can modulate the human fecal flora. Specific and

significant lachnospiraceogenic and bifidogenic prebioses were observed,

together with increased acetate, propionate, and butyrate production ac-

companied by enzyme activities that correspond with both the carbohydrate

utilization methodologies employed by these members of the microbiota

and the carbohydrate substrates available from the green kiwifruit itself.

215Modification of the Colonic Microbiota

4. KIWIFRUIT FERMENTATION OFFERS FUNCTIONALBENEFITS TO THE GUT

In addition to modulating microbial numbers and by-products,

fermentation of both green and gold kiwifruit has been shown to influence

gut microecology bymodulating the adhesion of different bacteria to the gut,

which is the first step in microbial colonization of the gut wall (Bavington &

Page, 2005; Parkar et al., 2010). These fermenta were found to increase the

proliferation of Bifidobacterium longum (Parkar et al., 2012), one of the probi-

otic organisms most commonly found in human feces (Malinen et al., 2002)

and further increased their adhesion to human intestinal epithelial cells. In the

gut, this would increase their chances of stable colonization. These adhesion

effects are consistent with previous work that showed that a pectin fraction

rich in galactose, arabinose, and galacturonic acid enhanced the adhesion

of Lactobacillus rhamnosus to Caco-2 cells in vitro, but inhibited the adhesion

of S. enterica (serovar Typhimurium; Parkar et al., 2010).

As well as organic acids, the microbiota are known to directly produce

antimicrobial substances, such as bacteriocins, which exhibit bactericidal ac-

tivity toward closely related strains (Riley & Wertz, 2002). Although no

work has yet linked the production of bacteriocins with the consumption

of kiwifruit, we know that kiwifruit consumption increases the numbers

of appropriate probiotic strains, and this can increase beneficial bacteriocins.

This, in turn, can augment the host resistance to allochthonous pathogens

(Tuohy, Rouzaud, Bruck, & Gibson, 2005).

In addition to an elevated production of bacteriocins to challenge

pathogen growth, increases in organic acids andmucin-degrading enzyme ac-

tivities associated with Bacteroidetes (Xu et al., 2003) and Bifidobacteria (Turroni

et al., 2010) in the kiwifruit-fermenting microbiota (Parkar et al., 2012) are

associated with either increased host antimicrobial peptide production

(organic acids; described in Chapter 17), competitive exclusion through

outcompeting for mucin colonization sites (Bacteroidetes, Bifidobacteria), or

outcompeting for epithelial binding sites (Bifidobacteria).

5. CONCLUSION

There is growing evidence that consumption of kiwifruit beneficially

modulates the colonic microbiota. Kiwifruit carbohydrates, vitamins, and

phytochemicals that escape host digestion are fermented by the microbiota,

216 Juliet Ansell et al.

changingmicrobial growth and by-product formation; and affecting binding

to colonization sites in the gut and the ability to directly or indirectly stim-

ulate immune cells. Therefore, through modulation of the microbiota,

kiwifruit consumption can affect many of the predominant factors which

collectively comprise the large intestinal system. This is likely to ultimately

result in increased large intestinal health and overall wellness.

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