Takeuchi Hayate, Matsuishi Takashi Fritz, Hayakawa Takashi
Division of Biosphere Science Graduate School of Environmental Science, Hokkaido University Sapporo Hokkaido Japan.
Global Center for Food, Land and Water Resources Faculty of Fisheries Sciences, Hokkaido University Hakodate Hokkaido Japan.
Ecol Evol. 2025 Aug 8;15(8):e71910. doi: 10.1002/ece3.71910. eCollection 2025 Aug.
Whales of the superfamily Physeteroidea, which includes the genera and , exhibit a unique visual defense mechanism involving the release of dark reddish-brown feces (locally called "tsunabi-ink" in Japan) into the water to obscure themselves from predators and other threats. However, the mechanism underlying pigmentation remains unknown. Because physeteroids possess an enlarged distal colon that retains fecal material, a possible explanation is that symbiont microbial metabolism contributes to the feces pigmentation. To investigate this, we provided a shotgun metagenomic catalog of gut microbiomes from the intestinal tracts of eight cetacean species, including two physeteroids: a sperm whale () and a pygmy sperm whale (). The colonic microbiome of physeteroids exhibited relatively high abundances of tryptophan metabolism genes, particularly indolepyruvate ferredoxin oxidoreductases ( and ), suggesting that physeteroids accumulate indole-3-pyruvate-derived pigments in their colons. Furthermore, bacterial members of the phyla Bacillota and Bacteroidota were identified in the physeteroid colon as primary taxa conferring heavy-metal resistance, which may be related to the primary predation of physeteroids on cephalopods, which bioaccumulate high levels of heavy metals. Prolonged fecal retention can expose gut microbes to chronic heavy-metal stress and colonize them as heavy metal-tolerant microbial communities, some of which may produce pigments to reduce their toxicity. Thus, we propose that tsunabi-ink is a metabolic byproduct of shifts in the gut microbial community, influenced by the host's digestive physiology and foraging behavior through sustained ecological interactions with gut symbionts. Moreover, we believe that further empirical investigation would validate this hypothesis.
抹香鲸总科的鲸鱼,包括 属和 属,展现出一种独特的视觉防御机制,即向水中释放深红褐色粪便(在日本当地称为“海啸墨汁”),以使自己躲避捕食者和其他威胁。然而,色素沉着的潜在机制仍然未知。由于抹香鲸类拥有一个扩大的远端结肠来留存粪便物质,一种可能的解释是共生微生物代谢促成了粪便的色素沉着。为了对此进行研究,我们提供了来自八种鲸类肠道的肠道微生物群落的鸟枪法宏基因组目录,其中包括两种抹香鲸类:一头抹香鲸( )和一头侏儒抹香鲸( )。抹香鲸类的结肠微生物群落表现出相对较高丰度的色氨酸代谢基因,尤其是吲哚丙酮酸铁氧还蛋白氧化还原酶( 和 ),这表明抹香鲸类在其结肠中积累吲哚 - 3 - 丙酮酸衍生的色素。此外,厚壁菌门和拟杆菌门的细菌成员在抹香鲸类结肠中被鉴定为赋予重金属抗性的主要类群,这可能与抹香鲸类主要捕食头足类动物有关,头足类动物会生物累积高水平的重金属。长时间的粪便留存会使肠道微生物暴露于慢性重金属压力下,并使它们定殖为耐重金属的微生物群落,其中一些群落可能会产生色素以降低其毒性。因此,我们提出海啸墨汁是肠道微生物群落变化的代谢副产物,受到宿主消化生理和觅食行为的影响,通过与肠道共生体的持续生态相互作用产生。此外,我们相信进一步的实证研究将验证这一假设。
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