Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
mBio. 2011 Apr 12;2(2). doi: 10.1128/mBio.00335-10. Print 2011.
Vibrio cholerae represents both an environmental pathogen and a widely distributed microbial species comprised of closely related strains occurring in the tropical to temperate coastal ocean across the globe (Colwell RR, Science 274:2025-2031, 1996; Griffith DC, Kelly-Hope LA, Miller MA, Am. J. Trop. Med. Hyg. 75:973-977, 2006; Reidl J, Klose KE, FEMS Microbiol. Rev. 26:125-139, 2002). However, although this implies dispersal and growth across diverse environmental conditions, how locally successful populations assemble from a possibly global gene pool, relatively unhindered by geographic boundaries, remains poorly understood. Here, we show that environmental Vibrio cholerae possesses two, largely distinct gene pools: one is vertically inherited and globally well mixed, and the other is local and rapidly transferred across species boundaries to generate an endemic population structure. While phylogeographic analysis of isolates collected from Bangladesh and the U.S. east coast suggested strong panmixis for protein-coding genes, there was geographic structure in integrons, which are the only genomic islands present in all strains of V. cholerae (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442-15447, 2009) and are capable of acquiring and expressing mobile gene cassettes. Geographic differentiation in integrons arises from high gene turnover, with acquisition from a locally co-occurring sister species being up to twice as likely as exchange with conspecific but geographically distant V. cholerae populations. IMPORTANCE Functional predictions of integron genes show the predominance of secondary metabolism and cell surface modification, which is consistent with a role in competition and predation defense. We suggest that the integron gene pool's distinctness and tempo of sharing are adaptive in allowing rapid conversion of genomes to reflect local ecological constraints. Because the integron is frequently the main element differentiating clinical strains (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442-15447, 2009) and its recombinogenic activity is directly stimulated by environmental stresses (Guerin E, et al., Science 324:1034, 2009), these observations are relevant for local emergence and subsequent dispersal.
霍乱弧菌既是一种环境病原体，也是一种广泛分布的微生物物种，由全球热带到温带沿海水域中密切相关的菌株组成（Colwell RR，Science 274:2025-2031, 1996；Griffith DC, Kelly-Hope LA, Miller MA, Am. J. Trop. Med. Hyg. 75:973-977, 2006；Reidl J, Klose KE, FEMS Microbiol. Rev. 26:125-139, 2002）。然而，尽管这意味着在不同的环境条件下进行了传播和生长，但如何在不受地理边界限制的情况下，从可能的全球基因库中成功组装局部种群，仍知之甚少。在这里，我们表明，环境中的霍乱弧菌拥有两个截然不同的基因库：一个是垂直遗传的，全球混合良好，另一个是本地的，能够快速跨越物种边界，产生地方性的种群结构。虽然对从孟加拉国和美国东海岸采集的分离株进行的系统地理学分析表明，编码蛋白的基因存在强烈的泛混合现象，但整合子存在地理结构，整合子是所有霍乱弧菌菌株中唯一存在的基因组岛（Chun J，等人，Proc. Natl. Acad. Sci. U. S. A. 106:15442-15447, 2009），并且能够获取和表达移动基因盒。整合子的地理分化源于高基因周转率，与来自本地共存的姐妹种的获得相比，与同种但地理上遥远的霍乱弧菌种群的交换可能性高两倍。重要性整合子基因的功能预测表明，它们主要参与次生代谢和细胞表面修饰，这与竞争和捕食防御作用一致。我们认为，整合子基因库的独特性和共享的速度是适应性的，允许快速转换基因组以反映本地生态限制。由于整合子通常是区分临床菌株的主要因素（Chun J，等人，Proc. Natl. Acad. Sci. U. S. A. 106:15442-15447, 2009），其重组活性直接受到环境压力的刺激（Guerin E，等人，Science 324:1034, 2009），因此这些观察结果与局部出现和随后的传播有关。
