Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria, the middle and lower parts by anoxygenic purple sulfur bacteria (Chromatiales) and green sulfur bacteria (Chlorobiales), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation and photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi. Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp. The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi-affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi. The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon.

中文翻译：

---

硫化物驱动的光养华中的微生物群落动力学和共存

泻湖在世界各地的海岸线上很常见，对于生物地球化学元素循环、沿海生物多样性、海岸侵蚀保护和蓝色碳封存具有重要意义。这些生态系统经常受到天气、潮汐和人类活动的干扰。在这里，我们调查了新英格兰的一个浅泻湖。微咸生态系统会释放硫化氢，特别是在物理干扰时，导致厌氧硫氧化光养生物大量繁殖。为了研究栖息地、微生物群落结构、组装和功能，我们进行了原位实验，研究了随时间推移的水华动态。光养微生物垫和永久或季节性分层水柱通常包含多种光养谱系，这些谱系根据它们的光、氧和营养偏好共存。我们描述了光养生物在河口浮游生物中的相似共存模式和生态位。水柱显示出氧气、pH 值、硫酸盐、硫化物和盐度的陡峭梯度。水华的上部以好氧光养蓝藻为主，中部和下部分别以厌氧紫硫细菌（Chromatiales）和绿硫细菌（Chlorobiales）为主。我们展示了来自五个细菌门的光养谱系的稳定共存，并展示了两种未培养的 Chlorobaculum 和 Prosthecochloris 物种的宏基因组组装基因组 (MAG)。除了参与硫氧化和光色素生物合成的基因外，MAG 还包含编码末端氧化酶的完整操纵子。宏基因组还包含许多与微病毒科病毒相关的重叠群，可能影响 Chlorobi。我们的数据表明，在水华中有一个短的硫循环，其中硫化物氧化光养生物产生的元素硫很可能被脱硫单胞菌还原为硫化物。硫化物的释放为厌氧硫氧化光养生物创造了一个栖息地，这反过来又为硫还原剂创造了一个小生境。这些行会之间强烈的共生作用显然驱动了一个短的硫循环，这可以解释水华的快速发展。Chlorobi 附属生物的快速生长和高生物量产量意味着所研究的绿色硫细菌谱系可以在缺氧栖息地中茁壮成长。在未培养的 Chlorobi 的 MAG 中发现的氧化酶证实了这种耐氧性。