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Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics.

ABSTRACT: How complex communities assemble through the animal's life, and how predictable the process is remains unexplored. Here, we investigate the forces that drive the assembly of rumen microbiomes throughout a cow's life, with emphasis on the balance between stochastic and deterministic processes. We analyse the development of the rumen microbiome from birth to adulthood using 16S-rRNA amplicon sequencing data and find that the animals shared a group of core successional species that invaded early on and persisted until adulthood. Along with deterministic factors, such as age and diet, early arriving species exerted strong priority effects, whereby dynamics of late successional taxa were strongly dependent on microbiome composition at early life stages. Priority effects also manifest as dramatic changes in microbiome development dynamics between animals delivered by C-section vs. natural birth, with the former undergoing much more rapid species invasion and accelerated microbiome development. Overall, our findings show that together with strong deterministic constrains imposed by diet and age, stochastic colonization in early life has long-lasting impacts on the development of animal microbiomes.

SUBMITTER: Furman O

PROVIDER: S-EPMC7170844 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics.

Furman Ori O Shenhav Liat L Sasson Goor G Kokou Fotini F Honig Hen H Jacoby Shamay S Hertz Tomer T Cordero Otto X OX Halperin Eran E Mizrahi Itzhak I

Nature communications 20200420 1

How complex communities assemble through the animal's life, and how predictable the process is remains unexplored. Here, we investigate the forces that drive the assembly of rumen microbiomes throughout a cow's life, with emphasis on the balance between stochastic and deterministic processes. We analyse the development of the rumen microbiome from birth to adulthood using 16S-rRNA amplicon sequencing data and find that the animals shared a group of core successional species that invaded early on ...[more]

PMID: 32312972

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Project description:BackgroundStocker cattle diet and management influence beef cattle performance during the finishing stage, but knowledge of the dynamics of the rumen microbiome associated with the host are lacking. A longitudinal study was conducted to determine how the feeding strategy from the stocker to the finishing stages of production affects the temporal dynamics of rumen microbiota. During the stocker phase, either dry hay or wheat pasture were provided, and three levels of monensin were administrated. All calves were then transported to a feedlot and received similar finishing diets with or without monensin. Rumen microbial samples were collected on d 0, 28, 85 during the stocker stage (S0, S28 and S85) and d 0, 14, 28, 56, 30 d before slaughter and the end of the trial during the finishing stage (F0, F14, F28, F56, Pre-Ba, and Final). The V4 region of the bacterial 16S rRNA gene of 263 rumen samples was sequenced.ResultsHigher alpha diversity, including the number of observed bacterial features and the Shannon index, was observed in the stocker phase compared to the finishing phase. The bacterial amplicon sequence variants (ASVs) differentiating different sampling time points were identified. Dietary treatments during the stocker stage temporally impact the dynamics of rumen microbiota. For example, shared bacteria, including Bacteroidales (ASV19) and Streptococcus infantarius (ASV94), were significantly higher in hay rumen on S28, S85, and F0, while Bacteroidaceae (ASV11) and Limivicinus (ASV15) were more abundant in wheat. Monensin affected rumen microbial composition at a specific time. Transportation to feedlot significantly influenced microbiome structure and diversity in hay-fed calves. Bacterial taxa associated with body weight were classified, and core microbiotas interacted with each other during the trial.ConclusionsIn summary, the temporal dynamics of the rumen microbiome in cattle at the stocker and finishing stage are influenced by multiple factors of the feeding strategy. Diet at the stocker phase may temporarily affect the microbial composition during this stage. Modulating the rumen microbiome in the steers at the stocker stage affects the microbial interactions and performance in the finishing stage.

Project description:The gut microbiome has far-reaching effects on host organism health, so understanding the processes that underlie microbial community assembly in the developing gut is a current research priority. Here, a holothurian (also known as sea cucumber; phylum Echinodermata) host is explored as a promising model system for studying the assembly of the gut microbiome. Holothurians have a unique capacity for evisceration (expulsion of the internal organs), followed by rapid regeneration of the gut, decoupling host ontogeny from gut tissue development and permitting experimental manipulation of the gut microbiome in mature host individuals. Here, evisceration was induced in the sea cucumber Sclerodactyla briareus, and regenerating stomach and intestine microbiomes were characterized before and on days 0, 13, 17, and 20 after evisceration using Illumina sequencing of 16S rRNA genes. Regenerating stomach and intestine tissues had microbial communities significantly different from those of mature tissues, with much higher alpha diversity and evenness of taxa in regenerating tissues. Despite immersion in a diverse pool of sediment and seawater microbes in flowthrough seawater aquaria, regenerating gut microbiomes differed at each stage of regeneration and displayed a highly similar community structure among replicates, providing evidence for deterministic host selection of a specific microbial consortium. Moreover, regenerating gut tissues acquired a microbiome that likely conferred energetic and immune advantages to the sea cucumber host, including microbes that can fix carbon and degrade invading pathogens.IMPORTANCE The gut microbiome is pertinent to many aspects of animal health, and there is a great need for natural but tractable experimental systems to examine the processes shaping gut microbiome assembly. Here, the holothurian (sea cucumber) Sclerodactyla briareus was explored as an experimental system to study microbial colonization in the gut, as S. briareus individuals have the ability to completely eviscerate and rapidly regenerate their digestive organs. After induced evisceration, microbial community assembly was characterized over 20 days in regenerating animals. This study demonstrated that colonization of the sea cucumber gut was deterministic; despite immersion in a diverse consortium of environmental microbes, a specific subset of microbes proliferated in the gut, including taxa that likely conferred energetic and immune advantages to the host. Sea cucumbers have the potential to revolutionize our understanding of gut microbiome assembly, as rapid and repeatable gut tissue regeneration provides a promising and tractable experimental system.

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Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics.

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Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics.

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