Fecal Methylmercury Correlates With Gut Microbiota Taxa in Pacific Walruses (Odobenus rosmarus divergens)

Abstract

Objectives: Methylmercury metabolism was investigated in Pacific walruses (Odobenus rosmarus divergens) from St. Lawrence Island, Alaska, United States.

Methods: Total mercury and methylmercury concentrations were measured in fecal samples and paired colon samples (n = 16 walruses). Gut microbiota composition and diversity were determined using 16S rRNA gene sequencing. Associations between fecal and colon mercury and the 24 most prevalent gut microbiota taxa were investigated using linear models.

Results: In fecal samples, the median values for total mercury, methylmercury, and %methylmercury (of total mercury) were 200 ng/g, 4.7 ng/g, and 2.5%, respectively, while in colon samples, the median values for the same parameters were 28 ng/g, 7.8 ng/g, and 26%, respectively. In fecal samples, methylmercury was negatively correlated with one Bacteroides genus, while members of the Oscillospirales order were positively correlated with both methylmercury and %methylmercury (of total mercury). In colon samples, %methylmercury (of total mercury) was negatively correlated with members of two genera, Romboutsia and Paeniclostridium.

Conclusions: Median %methylmercury (of total mercury) was 10 times higher in the colon compared to the fecal samples, suggesting that methylmercury was able to pass through the colon into systemic circulation. Fecal total mercury and/or methylmercury concentrations in walruses were comparable to some human studies despite differences in seafood consumption rates, suggesting that walruses excreted less mercury. There are no members (at this time) of the Oscillospirales order which are known to contain the genes to methylate mercury, suggesting the source of methylmercury in the gut was from diet and not in vivo methylation.

Keywords: Arctic; alpha diversity; colon; marine mammal; metabolism; microbiome; pinniped; stable isotopes of C and N.

FIGURE 1

The Pacific walrus (Odobenus rosmarus divergens) range, including St. Lawrence Island, Alaska, which lies in the migration path (source: Alaska Department of Fish and Game (ADFG), 2020).

FIGURE 2

Associations between the alpha diversity indices and fecal methylmercury (MeHg) (A–D) or %MeHg [of total mercury (THg)] (E–H) (both log₁₀-transformed), including (A,E) Shannon’s diversity index, (B,F) Simpson’s diversity index, (C,G) the observed number of amplicon sequence variants, and (D,H) Pielou’s measure of evenness. Each plot includes the linear regression line ± standard error of the regression line.

FIGURE 3

Associations between the relative abundance of gut microbiota amplicon sequence variants (ASVs, arcsine-square root transformed) and fecal methylmercury (MeHg) (A–C) or %MeHg [of total mercury (THg)] (D–F) (both log₁₀-transformed), including (A) genus UCG-005 (1) (family: Oscillospiraceae), (B) order Oscillospirales, (C) genus Bacteroides (family: Bacteroidaceae), (D) genus UCG-005 (1) (family: Oscillospiraceae), (E) order Oscillospirales, and (F) genus UCG-005 (2) (family: Oscillospiraceae) (n = 16 walruses). Each plot includes the linear regression line ± standard error of the regression line (see Table 4).

FIGURE 4

Associations between the relative abundance of gut microbiota amplicon sequence variants (arcsine-square root transformed) and colon %methylmercury (MeHg) [of total mercury (THg)] (log₁₀-transformed), including (A) genus Romboutsia (family: Peptostreptococcaceae) and (B) genus Paeniclostridium (family: Peptostreptococcaceae) (n = 16 walruses). Each plot includes the linear regression line ± standard error of the regression line (see Table 4).