Biogeographical Differences in the Influence of Maternal Microbial Sources on the Early Successional Development of the Bovine Neonatal Gastrointestinal tract.

Most studies that examine the microbial diversity of the gastrointestinal tract only look at one or two sample sites, usually the mouth, the rumen in ruminant animals, or the feces.  It can be difficult, expensive, invasive, or fatal to get samples from deep inside the intestinal tract; however many studies have pointed out that anatomical location and local environmental factors (like temperature, pH, host cells, nutrient availability, and exposure to UV light) can dramatically change a microbial community.  Thus, the microbes that we find in feces aren’t always what we would find in the stomach or along the intestines.

On top of that, certain microorganisms have been shown to closely associate with or attach to host cells lining the digestive tract, and the diversity of microbes next to host tissues can be different from what’s at the center of the intestines (the digesta).  This large, collaborative project took samples from nine different sites along the digestive tract of calves over the first 21 days of life to determine how body sites differed from each other, how sites changed over time as the calf matured, and how the lumen-associated bacteria would differ from the digesta-associated bacteria.

41598_2018_21440_Fig1_HTML
Figure 1 Mean bacterial diversity at the phylum level for maternal and calf lumen (A) and mucosal (B) samples.

Samples from the mothers were also taken to understand how maternal microbial influence would affect body sites over time.  One of the most interesting finds of the study regarded colostrum, which is the special and highly-nutritious milk produced in the first 48 hours or so after parturition (birth).  Colostrum milk possessed a high diversity of bacteria, and is not sterile as was once assumed.

Capture
Figure 1 (partial) Mean bacterial diversity at the phylum level for maternal and calf lumen (left) and mucosal (right) samples.

Not only that, but the bacterial community in colostrum had an impact on the bacterial community that developed along the calf digestive tract over time.  Calves received two doses of colostrum on the day of birth which had been aseptically collected from their dams and then fed to them, so that calves received milk but not the microbial influence of nursing and coming into contact with the dam.  After those two meals, calves were switched to milk replacer.  Surprisingly, the influence on the bacterial community wasn’t high on day one and then dropped off.  It increased over the first 21 days of life as bacterial communities from the digestive tract became more similar to bacterial communities found in colostrum (shown below).

colostrum
A poor-quality GIF, showing bacterial communities from the calf digestive tract (each other the colored shaped) becoming more similar to maternal colostrum (milk) samples (grey asterisk) over the first 21 days of life.

In addition, we found that bacteria in the digestive tract became more similar to maternal samples moving from one end of the digestive tract to the other. We speculated that bacterial communities need time to develop, especially in a neonate ruminant which doesn’t have a functional rumen yet.  A flap of skin at the base of the esophagus (called the esophageal groove) shunts food into the omasum, bypassing the rumen and the reticulum where bacteria and other microorganisms would otherwise thrive.  After briefly passing through the omasum, milk would pass through the abomasum which is a glandular stomach (like the human stomach).  Both of those features are obstacles for ingested microorganisms to get past, and it would take time, and distance, to recover.

GI tract
An equally poor-quality GIF, showing bacterial communities (colored shapes) from the calf digestive tract samples becoming more similar to maternal samples (grey asterisks) as one moves along the digestive tract.

Yeoman, C.J., Ishaq, S.L., Bichi , E., Olivo, S., Lowe, J., Aldridge, B.M. 2018. Biogeographical Differences in the Influence of Maternal Microbial Sources on the Early Successional Development of the Bovine Neonatal Gastrointestinal tract. Scientific Reports 8: 3197Article.

Abstract

The impact of maternal microbial influences on the early choreography of the neonatal calf microbiome were investigated. Luminal content and mucosal scraping samples were collected from ten locations in the calf gastrointestinal tract (GIT) over the first 21 days of life, along with postpartum maternal colostrum, udder skin, and vaginal scrapings. Microbiota were found to vary by anatomical location, between the lumen and mucosa at each GIT location, and differentially enriched for maternal vaginal, skin, and colostral microbiota. Most calf sample sites exhibited a gradual increase in α-diversity over the 21 days beginning the first few days after birth. The relative abundance of Firmicutes was greater in the proximal GIT, while Bacteroidetes were greater in the distal GIT. Proteobacteria exhibited greater relative abundances in mucosal scrapings relative to luminal content. Forty-six percent of calf luminal microbes and 41% of mucosal microbes were observed in at-least one maternal source, with the majority being shared with microbes on the skin of the udder. The vaginal microbiota were found to harbor and uniquely share many common and well-described fibrolytic rumen bacteria, as well as methanogenic archaea, potentially indicating a role for the vagina in populating the developing rumen and reticulum with microbes important to the nutrition of the adult animal.


Ishaq*, S.L., Bichi, E., Olivo, S.K., Lowe, J., Yeoman, C.J., Aldridge, B M. 2016. Influence of colostrum on the microbiological diversity of the developing bovine intestinal tract. Joint Annual Meeting, Salt Lake City, Utah, July 2016. (accepted talk)

 

 

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