microorganisms
Article
Does Organic Farming Increase Raspberry Quality, Aroma and
Beneficial Bacterial Biodiversity?
Daniela Sangiorgio
1,†
, Antonio Cellini
1,†
, Francesco Spinelli
1,
* , Brian Farneti
2
, Iuliia Khomenko
2
,
Enrico Muzzi
1
, Stefano Savioli
1
, Chiara Pastore
1
, María Teresa Rodriguez-Estrada
1
and Irene Donati
1,3
Citation: Sangiorgio, D.; Cellini, A.;
Spinelli, F.; Farneti, B.; Khomenko, I.;
Muzzi, E.; Savioli, S.; Pastore, C.;
Rodriguez-Estrada, M.T.; Donati, I.
Does Organic Farming Increase
Raspberry Quality, Aroma and
Beneficial Bacterial Biodiversity?
Microorganisms 2021, 9, 1617.
https://doi.org/10.3390/
microorganisms9081617
Academic Editor: Denis Faure
Received: 9 June 2021
Accepted: 2 July 2021
Published: 29 July 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1
Department of Agricultural and Food Sciences, University of Bologna, 40127 Bologna, Italy;
daniela.sangiorgio2@unibo.it (D.S.); antonio.cellini2@unibo.it (A.C.); enrico.muzzi@unibo.it (E.M.);
stefano_savioli@fastwebnet.it (S.S.); chiara.pastore@unibo.it (C.P.); maria.rodriguez@unibo.it (M.T.R.-E.);
irene.donati@zespri.com (I.D.)
2
Research and Innovation Center, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
brian.farneti@fmach.it (B.F.); iuliia.khomenko@fmach.it (I.K.)
3
Zespri Fresh Produce, 40132 Bologna, Italy
* Correspondence: francesco.spinelli3@unibo.it; Tel.: +39-051-2096443
† These authors contributed equally.
Abstract: Plant-associated microbes can shape plant phenotype, performance, and productivity.
Cultivation methods can influence the plant microbiome structure and differences observed in the
nutritional quality of differently grown fruits might be due to variations in the microbiome taxonomic
and functional composition. Here, the influence of organic and integrated pest management (IPM)
cultivation on quality, aroma and microbiome of raspberry (Rubus idaeus L.) fruits was evaluated.
Differences in the fruit microbiome of organic and IPM raspberry were examined by next-generation
sequencing and bacterial isolates characterization to highlight the potential contribution of the
resident-microflora to fruit characteristics and aroma. The cultivation method strongly influenced
fruit nutraceutical traits, aroma and epiphytic bacterial biocoenosis. Organic cultivation resulted in
smaller fruits with a higher anthocyanidins content and lower titratable acidity content in comparison
to IPM berries. Management practices also influenced the amounts of acids, ketones, aldehydes
and monoterpenes, emitted by fruits. Our results suggest that the effects on fruit quality could be
related to differences in the population of Gluconobacter, Sphingomonas, Rosenbergiella, Brevibacillus and
Methylobacterium on fruit. Finally, changes in fruit aroma can be partly explained by volatile organic
compounds (VOCs) emitted by key bacterial genera characterizing organic and IPM raspberry fruits.
Keywords: Rubus idaeus L.; VOCs; microbiome; volatilome; Gluconobacter; anthocyanins
1. Introduction
Raspberry (Rubus idaeus L.) is a highly valuable crop with a large agricultural potential,
both in Europe and worldwide. Raspberry consumer demand, as well as its cultivation,
have been steadily increasing in the past 20 years, with a further acceleration since 2010 [1].
Russia is the top producing country, with a production volume of 165,800 tonnes accounting
approx. for 20% of the world production [1]. Raspberry is also widely cultivated in other
European (Serbia, Poland) and north-American (Mexico, USA) countries [1,2].
Hedonic characteristics and nutraceutical properties of raspberry are the main drivers
of consumer appreciation. In fact, raspberry is rich in health-beneficial compounds, such as
flavonols, catechins, ascorbic acid and ellagic acid derivatives [3,4]. Additionally, more than
300 volatile organic compounds (VOCs) have been reported as constituents of raspberry
aroma [5], including alcohols, aldehydes, ketones, esters and terpenoids [6,7]. Among
the main aroma-active compounds (i.e., those with low perception threshold compared to
emission rates), C6 aldehydes (hexanal, hexenal isomers) and norisoprenoids (e.g., ionones)
are responsible for grassy and floral notes of raspberry fruit aroma [8].
Microorganisms 2021, 9, 1617. https://doi.org/10.3390/microorganisms9081617 https://www.mdpi.com/journal/microorganisms