Article pubs.acs.org/JAFC
Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Characterization of Polysaccharides from Feijoa Fruits (Acca sellowiana Berg.) and Their Utilization as Growth Substrates by Gut Commensal Bacteroides Species Tracey J. Bell,† Sarah L. Draper,† Manuela Centanni,‡ Susan M. Carnachan,† Gerald W. Tannock,‡,§,∥ and Ian M. Sims*,†,∥ †
Ferrier Research Institute, Victoria University of Wellington, 69 Gracefield Road, Lower Hutt 5040, New Zealand Department of Microbiology and Immunology and ∥Microbiome Otago, Department of Microbiology and Immunology, University of Otago, Post Office Box 56, Dunedin 9054, New Zealand § Riddet Institute Centre of Research Excellence, Palmerston North 4442, New Zealand
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ABSTRACT: Polysaccharides from feijoa fruit were extracted and analyzed; the composition of these polysaccharides conforms to those typically found in the primary cell walls of eudicotyledons. The two major polysaccharide extracts consisted of mainly pectic polysaccharides and hemicellulosic polysaccharides [xyloglucan (77%) and arabinoxylan (16%)]. A collection of commensal Bacteroides species was screened for growth in culture using these polysaccharide preparations and placed into five categories based on their preference for each substrate. Most of the species tested could utilize the pectic polysaccharides, but growth on the hemicellulose was more limited. Constituent sugar and glycosyl linkage analysis showed that species that grew on the hemicellulose fraction showed differences in their preference for the two polysaccharides in this preparation. Our data demonstrate that the members of the genus Bacteroides show differential hydrolysis of pectic polysaccharides, xyloglucan, and arabinoxylan, which might influence the structure and metabolic activities of the microbiota in the human gut. KEYWORDS: Acca sellowiana, feijoa, cell wall, polysaccharide, Bacteroides, gut microbiota
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INTRODUCTION Feijoa or pineapple guava (Acca sellowiana) is one of three species of genus Acca (formerly Feijoa) all endemic to South America.1 While not a true guava, feijoas are members of the Myrtoid subgroup1,2 of Myrtaceae, which also includes the tropical (Psidium guajava) and strawberry or cherry (Psidium littorale) guavas. Feijoa is grown widely in New Zealand, where considerable effort has been made to develop different varieties particularly to overcome self-incompatibility, extend the climate types, and lengthen the season in which it will grow; the fruit ripens in autumn. Most of the research published on the bioactive components of feijoa has focused on lowmolecular-weight natural products and their pharmacology.3 However, feijoa is high in dietary fiber, with the edible flesh of the fruit providing about 4 g of fiber.3 The main components of dietary fiber in fruit are polysaccharides that make up the plant cell wall.4 The high dietary fiber content of feijoa fruit is of particular interest in relation to a potential prebiotic effect in the human colon, where the resident microbial community (microbiota) is fueled by dietary components indigestible to human processes.5 A differential prebiotic effect might be useful if plant polysaccharides could be used as dietary interventions to correct dysbioses reported to be associated with particular human diseases and conditions.6 We have previously shown that Bacteroides species differentially utilize xylose-rich polysaccharides with differing structural complexity.7 More recently, Li et al.8 showed that Bacteroides thetaiotamicron grew on a pectic polysaccharide isolated from mulberry fruit, but Bacteroides ovatus and Bacteroides fragilis did not. Bacteroides species are common in the human colon and © XXXX American Chemical Society
have large genomes, encoding a substantial array of degradative pathways associated with polysaccharide utilization.9 As such, Bacteroides are primary degraders of plant polysaccharides in the gut, benefiting themselves and other bacterial species through metabolic cooperation, including syntrophy.10,11 Knowledge of polysaccharide composition and structure is a prerequisite for understanding differential prebiotic effects and, most importantly, substrate preferences (the order in which substances are used for bacterial growth). In this study, we isolated pectic and hemicellulosic polysaccharide fractions from the pulp of ripe feijoa fruit and characterized their composition and linkage structures. We tested the ability of common human bowel Bacteroides species to utilize these two fractions as growth substrates. We found that differential degradation and growth of these species occurred on these substrates and that certain species have a preference for specific hemicellulosic polysaccharides.
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MATERIALS AND METHODS
Plant Material. Ripe feijoas were collected in May 2016 from a local market, halved, with the flesh inside composed mostly of mesocarp and endocarp (including the seeds), collected, and stored frozen before processing. Preparation of Substrates from Feijoa Fruits. Frozen feijoa pulp (200 g) was thawed, mixed with ethanol (650 mL), and Received: September 17, 2018 Revised: November 19, 2018 Accepted: November 21, 2018
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DOI: 10.1021/acs.jafc.8b05080 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Article
Journal of Agricultural and Food Chemistry
medium7,12 containing 2 g L−1 of the specific pectic or hemicellulosic polysaccharide fraction. All media, with or without a carbohydrate source, were filter-sterilized (0.45 μm pore size) and pre-reduced before inoculation with bacterial cultures. Three technical replicates and two biological replicates were carried out for each species studied. Optical density (OD600) was measured after 48 h of incubation at 37 °C in anaerobiosis. Spent culture supernatants were collected after centrifugation of samples at 14500g for 5 min and stored at −80 °C for subsequent carbohydrate analysis. Unpaired t tests were performed to compare the optical densities of bacterial cultures grown in the presence and absence of the carbohydrate substrate, using GraphPad Prism, version 7.0b (GraphPad Software, La Jolla, CA, U.S.A.; www.graphpad.com), considering a p value of
