Tolutope Akeju, Andriy Sheremet, Angela V. Smirnova, Daniel Yakimenka, Jamie Lee-Inwood, María Soto, Abdallah Mohamed, Aloyce Mwambwiga, Julio Mercader, Peter F. Dunfield
{"title":"Microbial starch degradation in arid soil: Community dynamics, environmental influences, and archaeological implications","authors":"Tolutope Akeju, Andriy Sheremet, Angela V. Smirnova, Daniel Yakimenka, Jamie Lee-Inwood, María Soto, Abdallah Mohamed, Aloyce Mwambwiga, Julio Mercader, Peter F. Dunfield","doi":"10.1016/j.soilbio.2025.109882","DOIUrl":null,"url":null,"abstract":"Starch is the primary energy storage compound in plants, and the most important carbohydrate in the human diet. Intact starch granules have been found in archaeological contexts, suggesting that starch may be recalcitrant to degradation in certain conditions. We identified microbial communities that degraded tuber starch in arid soils from Oldupai Gorge, Tanzania, and assessed their dependence on moisture, O<sub>2</sub>, and starch purity. Laboratory soil microcosms were amended with ground native <em>Ipomoea longituba</em> tubers or purified starch from <em>Solanum tuberosum</em> (common potato), which both contain starches of B-type crystallinity. Sequencing of 16S rRNA and 18S rRNA genes, DNA-stable isotope probing with <sup>13</sup>C labelled starch, and metagenomic analysis of amylases all indicated that starch was metabolised by diverse bacteria belonging mostly to the phyla <em>Actinomycetota</em> and <em>Bacillota (Firmicutes)</em>, and by <em>Ascomycota</em> fungi. Some of the starch-degrading <em>Actinomycetota</em> were also enriched in the rhizosphere of field <em>Ipomoea longituba</em> plants. Some microbes responded to both substrates, while others responded only to one. Members of the genus <em>Streptomyces</em> were stimulated by potato starch but not <em>Ipomoea longituba</em> tuber material, while members of the genus <em>Bacillus</em> were stimulated by <em>Ipomoea longituba</em> tuber but not potato starch. The use of purified starch in experiments therefore did not fully reproduce the complex interactions between plant-derived starch and soil microbial communities. Although starch purity, soil moisture and pO<sub>2</sub>, and microbial community all affected starch metabolism, visible starch granules were always rapidly destroyed, even when subsequent respiration of the starch material was severely limited. Native <em>Ipomoea longituba</em> starch granules were destroyed within a few days in all treatments. Our results therefore suggest that long-term preservation of native, unmodified starch granules in soils over long time periods is unlikely even under very harsh conditions. These results provide some guidance for designing future studies into starch preservation mechanisms.","PeriodicalId":21888,"journal":{"name":"Soil Biology & Biochemistry","volume":"559 1","pages":"109882"},"PeriodicalIF":9.8000,"publicationDate":"2025-06-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Soil Biology & Biochemistry","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1016/j.soilbio.2025.109882","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"SOIL SCIENCE","Score":null,"Total":0}
引用次数: 0
Abstract
Starch is the primary energy storage compound in plants, and the most important carbohydrate in the human diet. Intact starch granules have been found in archaeological contexts, suggesting that starch may be recalcitrant to degradation in certain conditions. We identified microbial communities that degraded tuber starch in arid soils from Oldupai Gorge, Tanzania, and assessed their dependence on moisture, O2, and starch purity. Laboratory soil microcosms were amended with ground native Ipomoea longituba tubers or purified starch from Solanum tuberosum (common potato), which both contain starches of B-type crystallinity. Sequencing of 16S rRNA and 18S rRNA genes, DNA-stable isotope probing with 13C labelled starch, and metagenomic analysis of amylases all indicated that starch was metabolised by diverse bacteria belonging mostly to the phyla Actinomycetota and Bacillota (Firmicutes), and by Ascomycota fungi. Some of the starch-degrading Actinomycetota were also enriched in the rhizosphere of field Ipomoea longituba plants. Some microbes responded to both substrates, while others responded only to one. Members of the genus Streptomyces were stimulated by potato starch but not Ipomoea longituba tuber material, while members of the genus Bacillus were stimulated by Ipomoea longituba tuber but not potato starch. The use of purified starch in experiments therefore did not fully reproduce the complex interactions between plant-derived starch and soil microbial communities. Although starch purity, soil moisture and pO2, and microbial community all affected starch metabolism, visible starch granules were always rapidly destroyed, even when subsequent respiration of the starch material was severely limited. Native Ipomoea longituba starch granules were destroyed within a few days in all treatments. Our results therefore suggest that long-term preservation of native, unmodified starch granules in soils over long time periods is unlikely even under very harsh conditions. These results provide some guidance for designing future studies into starch preservation mechanisms.
期刊介绍:
Soil Biology & Biochemistry publishes original research articles of international significance focusing on biological processes in soil and their applications to soil and environmental quality. Major topics include the ecology and biochemical processes of soil organisms, their effects on the environment, and interactions with plants. The journal also welcomes state-of-the-art reviews and discussions on contemporary research in soil biology and biochemistry.