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Changes in Rumen Bacterial and Archaeal Communities Over the Transition Period in Primiparous Holstein Dairy Cows

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Changes in Rumen Bacterial and Archaeal Communities Over the Transition Period in Primiparous Holstein Dairy Cows Changes in rumen bacterial and archaeal communities over the transition period in primiparous Holstein dairy cows Zhu, Zhigang; Kristensen, Lise; Difford, Gareth F.; Poulsen, Morten; Noel, Samantha J.; Abu Al-Soud, Waleed; Sørensen, Søren Johannes; Lassen, Jan; Løvendahl, Peter; Højberg, Ole Published in: Journal of Dairy Science DOI: 10.3168/jds.2017-14366 Publication date: 2018 Document version Publisher's PDF, also known as Version of record Document license: CC BY-NC-ND Citation for published version (APA): Zhu, Z., Kristensen, L., Difford, G. F., Poulsen, M., Noel, S. J., Abu Al-Soud, W., Sørensen, S. J., Lassen, J., Løvendahl, P., & Højberg, O. (2018). Changes in rumen bacterial and archaeal communities over the transition period in primiparous Holstein dairy cows. Journal of Dairy Science, 101(11), 9847-9862. https://doi.org/10.3168/jds.2017-14366 Download date: 25. Sep. 2021 J. Dairy Sci. 101:9847–9862 https://doi.org/10.3168/jds.2017-14366 © 2018, The Authors. Published by FASS Inc. and Elsevier Inc. on behalf of the American Dairy Science Association®. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Changes in rumen bacterial and archaeal communities over the transition period in primiparous Holstein dairy cows Zhigang Zhu,*1 Lise Kristensen,† Gareth F. Difford,† Morten Poulsen,* Samantha J. Noel,* Waleed Abu Al-Soud,‡ Søren J. Sørensen,‡ Jan Lassen,† Peter Løvendahl,† and Ole Højberg*1 *Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark †Center for Quantitative Genetics and Genomics, Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark ‡Department of Biology, Faculty of Science, University of Copenhagen, DK-2100 Copenhagen, Denmark ABSTRACT INTRODUCTION In the present study, we hypothesized that the ru- The dairy cow transition period, defined as 3 wk men bacterial and archaeal communities would change before to 3 wk after parturition, is characterized by significantly over the transition period of dairy cows, dramatic physiological changes and imposes severe mainly as an adaptation to the classical use of low-grain challenges on the animal for maintaining positive nutri- prepartum and high-grain postpartum diets. Bacterial ent and energy balances (Bell, 1995; Ingvartsen, 2006). 16S rRNA gene amplicon sequencing of rumen samples In ruminants, dietary carbohydrates are fermented by from 10 primiparous Holstein dairy cows revealed no rumen microbes into short-chain fatty acids (SCFA), changes over the transition period in relative abun- which are the major energy source for the host animal dance of genera such as Ruminococcus, Butyrivibrio, (Reynolds et al., 1988). During the prepartum period, Clostridium, Coprococcus, and Pseudobutyrivibrio. feed intake is typically low but still covering the energy However, other dominant genus-level taxa, such as Pre- needs of the cow. Postpartum, the demands for glucose, votella, unclassified Ruminococcaceae, and unclassified AA, and fatty acids are dramatically increased but the Succinivibrionaceae, showed distinct changes in relative slow increase in feed intake cannot satisfy the animal’s abundance from the prepartum to the postpartum nutrient and energy needs (Bell, 1995). A period of period. Overall, we observed individual fluctuation pat- negative energy balance is therefore encountered by terns over the transition period for a range of bacterial many cows during early lactation (Drackley, 1999), taxa that, in some cases, were correlated with observed where rates of hepatic gluconeogenesis and adipose fat changes in the rumen short-chain fatty acids profile. mobilization are greatly accelerated, potentially leading Combined results from clone library and terminal- to ketosis or fatty liver development. To help alleviate restriction fragment length polymorphism (T-RFLP) the negative energy balance and sustain high milk pro- analyses, targeting the methyl-coenzyme M reductase duction, the diet composition (roughage-to-concentrate α-subunit (mcrA) gene, revealed a methanogenic ar- ratio) and amount is commonly adjusted postpartum. chaeal community dominated by the Methanobacte- For the rumen bacterial community, high-grain di- riales and Methanomassiliicoccales orders, particularly ets typically induce a decline in diversity as well as the genera Methanobrevibacter, Methanosphaera, and an increase in starch-degrading and lactate-utilizing Methanomassiliicoccus. As observed for the bacterial or propionate-producing members of the genera Pre- community, the T-RFLP patterns showed significant votella, Streptococcus, Selenomonas, and Megasphaera shifts in methanogenic community composition over and a decrease in fibrolytic members of Butyrivibrio, the transition period. Together, the composition of the Ruminococcus, and Fibrobacter (Tajima et al., 2001; rumen bacterial and archaeal communities exhibited Fernando et al., 2010; Petri et al., 2013). Consequently, changes in response to particularly the dietary changes dietary changes may alter the rumen fermentation of dairy cows over the transition period. characteristics, such as SCFA production rate and pro- Key words: rumen bacteria, archaea, Illumina MiSeq, file (relative proportions of mainly acetate, propionate, terminal-RFLP, transition period and butyrate), which may again affect feed efficiency of the cow (Wang et al., 2012). Compared with the rumen bacterial community, the Received December 29, 2017. archaeal community is less diverse and, based on small Accepted July 3, 2018. 1 Corresponding authors: zhigang.zhu8800@gmail .com and ole. subunit ribosomal RNA analyses, the domain Archaea hojberg@ anis .au .dk has been reported to comprise only 0.5 to 2.5% of the 9847 9848 ZHU ET AL. entire rumen microbial community (Prokarya and Eu- response to dietary changes over the transition period karya) in domestic ruminants (Lin et al., 1997; Jeya- may lead to strategies to, potentially, manipulate the nathan et al., 2011). Moreover, the rumen Archaea is rumen microbiome and improve the health and nutri- represented almost solely by the Euryarchaeota phylum, tional status of primiparous cows in their first transi- covering all methanogens, and seems to be dominated tion period as well as later in life. by relatively few species within the Methanobrevibacter and Methanosphaera genera and the Methanomassili- MATERIALS AND METHODS icoccales order in ruminants across animal species, diet type, and geographical location (Jeyanathan et al., Animals, Diets, and Rumen Sampling 2011; Sirohi et al., 2013; Henderson et al., 2015). It should be kept in mind, however, that methanogens, The animal experimental procedure was performed although low in total numbers, are the main hydrogen according to a protocol approved by The Animal Ex- scavengers of the rumen and, as such, are key players periments Inspectorate, Danish Veterinary and Food in driving fermentation processes. The dynamics of not Administration, Ministry of Environment and Food only the bacterial, but also the methanogenic archaeal, of Denmark (approval number 2016-15-0201-00959). community of the rumen may therefore be crucial for The study included 10 primiparous Holstein cows with dairy cows, particular in critical life phases such as the close predicted calving dates, housed at a research farm transition period, when the animals are highly depen- (Danish Cattle Research Centre; www .DKC -Foulum dent on optimal energy metabolism. .dk). All cows were fed ad libitum with a low-grain Advanced sequencing technologies have enabled (high-forage) prepartum and a high-grain (low-forage) in-depth analysis of microbiomes (composition and postpartum diet (Table 1), and had free access to function). It has been demonstrated that the rumen drinking water. Feed intake data of the individual cows microbiome of dairy cows is dynamic and changes ac- were recorded automatically at each visit to the feeders cording to, for example, age (Jami et al., 2013; Rey et (Insentec B.V., Marknesse, the Netherlands; Supple- al., 2014), parity (Pitta et al., 2014a; Lima et al., 2015), mental Figure S1; https: / / doi .org/ 10 .3168/ jds .2017 and lactation cycle stage (Jewell et al., 2015), and -14366). Gestating cows were grouped in a barn with distinct prepartum to postpartum shifts in the rumen straw bedding. After calving, the cows were moved in- bacterial community composition have been observed dividually to a barn for lactating cows, equipped with (Mohammed et al., 2012; Wang et al., 2012; Pitta et a voluntary milking station (VMS, DeLaval, Tumba, al., 2014a; Lima et al., 2015). Most of the studies in- Sweden). The cows were offered a limited amount of vestigating the rumen microbiota over the transition concentrate when visiting the milking robot. Rumen period have focused on Bacteria (Mohammed et al., samples (7 per cow, 70 in total) were taken once a week 2012; Wang et al., 2012; Pitta et al., 2014a; Lima et al., after morning feeding (between 0900 and 1000 h after 2015; Zhu et al., 2017). For the present study, as in only feeding) for 7 consecutive weeks according to the sam- one other study (Dieho et al., 2017), we included not pling scheme shown in Figure 1. Because the expected only Bacteria, but also Archaea, hypothesizing that the and actual day of parturition differed, the cows were composition of both domains changes over the transition unintentionally sampled unevenly relative to parturi- period as an adaptation to mainly the dietary changes, tion. Consequently, cow 1 contributed
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