Dairy Production and the Rumen Microbiome: Research Directions in a Challenging Future

Ruminants' milk provides immense benefits as a rich source of nutrients, and plays a central role in ensuring food security for millions of people. However, these benefits are accompanied by notable drawbacks associated with its production, and with ruminant production more generally. Globally, dairy products account for around 11% of the protein in human diet, making milk the largest contributor of protein from animal sources. The role of milk-producing livestock in ensuring the livelihood of subsistence farmers in low- and middle-income countries must also be considered. Global milk production is projected to grow by 1.8% annually over the next 10 years 1. This growth will be achieved partly through higher yields per lactating animal and partly through increased numbers, particularly in regions experiencing growing demand, such as Sub-Saharan Africa, India, and Pakistan 1. However, dairy production significantly impacts the environment, affecting several biophysical planetary boundaries 2, 3. Dairy ruminants contribute to climate change and affect the biogeochemical flows of nitrogen and phosphorus, land system, and freshwater. These are all boundaries that are considered to be outside of the planet's safe operating space 4. Ruminants depend on microbes for their physiology. These host-associated microbes, in particular those in the rumen and other sections of the gastrointestinal tract, are responsible for both the capacity of ruminants to produce nutritious food from plant resources nonedible by humans, and also for the negative impacts on the environment attributed to ruminant farming, such as the production of methane, a greenhouse gas. The study of the rumen microbiota has long been recognized as key for improving production, health, and wellbeing of ruminants. Since the pioneer studies of Robert Hungate 5 more than 80 years ago, this has been an active area of research, and the knowledge acquired on the rumen microbiota over the years is readily applied in practice. This has led to improved management practices and nutritional programs and has been used to design intervention strategies, such as additives and direct-fed microbials, for specific purposes. More recently, the development and combined use of high-throughput omics techniques has accelerated the pace of discovery and understanding of the rumen microbiome and its interactions with the host 6. This progress is set to continue, offering a promising outlook for addressing sustainability in ruminant production through a microbiome-based approach. However, information on the rumen microbiome is still fragmented as it is obtained from a limited number of production systems—generally high-producing ones—a handful of breeds, and mainly temperate climates. Overcoming these hurdles is essential to ensure that knowledge of the rumen microbiome can be put into practice and can have a global impact. The deposit in public repositories of sequenced and other omics data is a requirement of most scientific journals and adherence to open science practices is increasingly mandatory by research funders. However, although the adoption of open science in animal science and animal microbiome research is certainly on the rise 7, the metadata necessary to make ruminant-microbiome data reusable often remains incomplete 8. For example, basic information such as age, sex or breed is missing in about half of the samples deposited in public repositories. In addition, assignation of the data to a ruminant species is not always indicated and the data have to be manually recovered 8. To address these issues, guidelines for the reporting of host-associated microbiomes have been developed 9 as well as templates to capture metadata information from ruminants are used in large scale projects (e.g., EU Horizon HoloRuminant). Adoption of these practices are necessary for making the data compliant with FAIR (Findable, Accessible, Interoperable, and Reusable) principles 10 and allow creation of integrated, rumen-specific databases. The microbiome of Holstein breed is the most widely represented in the literature and in public repositories 8. This is not surprising given the economic importance of this breed in milk production. Dairy cows account for ∼80% of the milk produced worldwide, with Holstein representing ∼65% of the milk produced by cattle. In contrast, other dairy cattle breeds, including local and crossbred, are underrepresented. The same is true of dairy buffalos, goats, and sheep that are also underrepresented. In addition, up to 90% of existing data come from Europe, China, North America, and Australasia whereas information from other regions of the word with large populations of dairy animals and varied production systems in terms of available diets and climate conditions is scarce or nonexistent 8. Sustainability is a relatively new goal in ruminant milk production. Microbiome knowledge has contributed largely to improvements in efficiency, resulting in a reduced environmental footprint of dairy products. Modulating the microbiome as a way to enhance feed efficiency will continue to be important in dairy production, particularly in low-yield systems. Nevertheless, microbiome research should encompass other phenotypic targets in dairy ruminants to be able to address sustainability challenges due to emerging global changes. Rising temperatures and CO2 levels in the atmosphere are unfavorably changing the nutritional composition and digestibility of forages 11. In addition, advancing desertification and droughts are negatively affecting feed production 12, with carry-over effects observed several years after drought episodes 13. High-producing dairy cows are particularly susceptible to heat stress 12, 14 and the combined negative effect of heat stress on intake, reproductive performance, and health is expected to reduce production in coming decades (5%–25% depending on parameters and models chosen) 12, 15. The vast majority of ruminants are in grazing and mixed crop-livestock systems, with about 90% of the world's milk being produced in mixed systems 12, 16. In the tropical and subtropical regions is where the largest concentration of ruminants are found and it is where the numbers are expected to increase as well (https://www.fao.org/faostat/; 1). Under optimal conditions, high-producing dairy cows have microbiomes that efficiently harvest energy from feeds, but these microbiomes are less diverse 17. In contrast, under stressful situations such as heat or dietary modifications as mentioned above, these animals are less robust. The rumen microbiota with its rapid adaptability, genetic plasticity, and resilience, may contribute to the robustness of dairy animals and therefore to a sustainable efficiency in dairy systems 18. However, traits in the microbiome that are associated with better resistance to heat stress, dietary variations, and plant toxicity, to name some, should be given greater attention as these stressful situations are expected to increase in the near future. Transforming rumen microbiome knowledge into practical solutions for the dairy production sector can be accelerated through coordination and sharing of resources. Large international projects such as HoloRuminant are producing extensive datasets and analytical tools that will be publicly available. However, no single project is capable of capturing the full range of microbial diversity worldwide, given the myriad combinations of host genetics, as well as local and temporal variations in climate, feed resources, and production systems. Global initiatives such as the World Microbiome Partnership or the Rumen Microbial Genomics Network could provide a forum for dialog to facilitate the harmonization and coordination required to create comprehensive global rumen-specific databases. These databases and analytical tools should contain information on all microbial groups interacting within the rumen microbiome. The influence of eukaryotes, such as anaerobic fungi and ciliate protozoa, on the functioning of the ecosystem is often overlooked, but could have significant implications 19, 20. Investing in these actions will have a positive impact on innovation in the dairy sector, which, with the right policies and interventions, may contribute to its sustainability. Diego P. Morgavi: conceptualization, writing – original draft. Funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No. 101000213-HoloRuminant is gratefully acknowledged. This work was supported by the European Union's Horizon 2020 research and innovation programme (Grant 101000213). The author declares no conflicts of interest. Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.