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Microbiome processing of organic nitrogen input supports growth and cyanotoxin production of Microcystis aeruginosa cultures
The ISME Journal ( IF 10.8 ) Pub Date : 2024-05-08 , DOI: 10.1093/ismejo/wrae082 Wei Li 1 , David Baliu-Rodriguez 1, 2 , Sanduni H Premathilaka 2 , Sharmila I Thenuwara 2 , Jeffrey A Kimbrel 1 , Ty J Samo 1 , Christina Ramon 1 , Erik Anders Kiledal 3 , Sara R Rivera 3 , Jenan Kharbush 3 , Dragan Isailovic 2 , Peter K Weber 1 , Gregory J Dick 3, 4 , Xavier Mayali 1
The ISME Journal ( IF 10.8 ) Pub Date : 2024-05-08 , DOI: 10.1093/ismejo/wrae082 Wei Li 1 , David Baliu-Rodriguez 1, 2 , Sanduni H Premathilaka 2 , Sharmila I Thenuwara 2 , Jeffrey A Kimbrel 1 , Ty J Samo 1 , Christina Ramon 1 , Erik Anders Kiledal 3 , Sara R Rivera 3 , Jenan Kharbush 3 , Dragan Isailovic 2 , Peter K Weber 1 , Gregory J Dick 3, 4 , Xavier Mayali 1
Affiliation
Nutrient-induced blooms of the globally abundant freshwater toxic cyanobacterium Microcystis cause worldwide public and ecosystem health concerns. The response of Microcystis growth and toxin production to new and recycled nitrogen (N) inputs, and the impact of heterotrophic bacteria in the Microcystis phycosphere on these processes are not well understood. Here, using microbiome transplant experiments, cyanotoxin analysis, and nanometer-scale stable isotope probing to measure N incorporation and exchange at single cell resolution, we monitored the growth, cyanotoxin production, and microbiome community structure of several Microcystis strains grown on amino acids or proteins as the sole N source. We demonstrate that the type of organic N available shaped the microbial community associated with Microcystis, and external organic N input led to decreased bacterial colonization of Microcystis colonies. Our data also suggest that certain Microcystis strains could directly uptake amino acids, but with lower rates than heterotrophic bacteria. Toxin analysis showed that biomass-specific microcystin production was not impacted by N source (i.e., nitrate, amino acids or protein) but rather by total N availability. Single-cell isotope incorporation revealed that some bacterial communities competed with Microcystis for organic N, but other communities promoted increased N uptake by Microcystis, likely through ammonification or organic N modification. Our laboratory culture data suggest that organic N input could support Microcystis blooms and toxin production in nature, and Microcystis-associated microbial communities likely play critical roles in this process by influencing cyanobacterial succession through either decreasing (via competition) or increasing (via biotransformation) N availability, especially under inorganic N scarcity.
中文翻译:
有机氮输入的微生物组处理支持铜绿微囊藻培养物的生长和蓝藻毒素的产生
全球丰富的淡水有毒蓝藻微囊藻的营养引起的水华引起了全世界公众和生态系统健康的担忧。微囊藻生长和毒素产生对新的和回收的氮(N)输入的反应,以及微囊藻藻圈中异养细菌对这些过程的影响尚不清楚。在这里,我们利用微生物组移植实验、蓝藻毒素分析和纳米级稳定同位素探测来测量单细胞分辨率下的氮掺入和交换,监测了几种在氨基酸或蛋白质上生长的微囊藻菌株的生长、蓝藻毒素产生和微生物组群落结构作为唯一的氮源。我们证明,可用有机氮的类型塑造了与微囊藻相关的微生物群落,外部有机氮输入导致微囊藻菌落的细菌定植减少。我们的数据还表明,某些微囊藻菌株可以直接摄取氨基酸,但摄取率低于异养细菌。毒素分析表明,生物质特异性微囊藻毒素的产生不受氮源(即硝酸盐、氨基酸或蛋白质)的影响,而是受总氮可用性的影响。单细胞同位素掺入显示,一些细菌群落与微囊藻竞争有机氮,但其他群落可能通过氨化或有机氮修饰促进微囊藻增加氮吸收。 我们的实验室培养数据表明,有机氮输入可以支持自然界中微囊藻的繁殖和毒素的产生,并且微囊藻相关的微生物群落可能在此过程中发挥关键作用,通过减少(通过竞争)或增加(通过生物转化)氮来影响蓝藻的演替。可用性,特别是在无机氮缺乏的情况下。
更新日期:2024-05-08
中文翻译:
有机氮输入的微生物组处理支持铜绿微囊藻培养物的生长和蓝藻毒素的产生
全球丰富的淡水有毒蓝藻微囊藻的营养引起的水华引起了全世界公众和生态系统健康的担忧。微囊藻生长和毒素产生对新的和回收的氮(N)输入的反应,以及微囊藻藻圈中异养细菌对这些过程的影响尚不清楚。在这里,我们利用微生物组移植实验、蓝藻毒素分析和纳米级稳定同位素探测来测量单细胞分辨率下的氮掺入和交换,监测了几种在氨基酸或蛋白质上生长的微囊藻菌株的生长、蓝藻毒素产生和微生物组群落结构作为唯一的氮源。我们证明,可用有机氮的类型塑造了与微囊藻相关的微生物群落,外部有机氮输入导致微囊藻菌落的细菌定植减少。我们的数据还表明,某些微囊藻菌株可以直接摄取氨基酸,但摄取率低于异养细菌。毒素分析表明,生物质特异性微囊藻毒素的产生不受氮源(即硝酸盐、氨基酸或蛋白质)的影响,而是受总氮可用性的影响。单细胞同位素掺入显示,一些细菌群落与微囊藻竞争有机氮,但其他群落可能通过氨化或有机氮修饰促进微囊藻增加氮吸收。 我们的实验室培养数据表明,有机氮输入可以支持自然界中微囊藻的繁殖和毒素的产生,并且微囊藻相关的微生物群落可能在此过程中发挥关键作用,通过减少(通过竞争)或增加(通过生物转化)氮来影响蓝藻的演替。可用性,特别是在无机氮缺乏的情况下。