Lee Justin, Malmberg Jennifer L, Wood Britta A, Hladky Sahaja, Troyer Ryan, Roelke Melody, Cunningham Mark, McBride Roy, Vickers Winston, Boyce Walter, Boydston Erin, Serieys Laurel, Riley Seth, Crooks Kevin, VandeWoude Sue
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
The Pirbright Institute, Pirbright, Surrey, United Kingdom.
J Virol. 2017 Feb 14;91(5). doi: 10.1128/JVI.02134-16. Print 2017 Mar 1.
Owing to a complex history of host-parasite coevolution, lentiviruses exhibit a high degree of species specificity. Given the well-documented viral archeology of human immunodeficiency virus (HIV) emergence following human exposures to simian immunodeficiency virus (SIV), an understanding of processes that promote successful cross-species lentiviral transmissions is highly relevant. We previously reported natural cross-species transmission of a subtype of feline immunodeficiency virus, puma lentivirus A (PLVA), between bobcats () and mountain lions () for a small number of animals in California and Florida. In this study, we investigate host-specific selection pressures, within-host viral fitness, and inter- versus intraspecies transmission patterns among a larger collection of PLV isolates from free-ranging bobcats and mountain lions. Analyses of proviral and viral RNA levels demonstrate that PLVA fitness is severely restricted in mountain lions compared to that in bobcats. We document evidence of diversifying selection in three of six PLVA genomes from mountain lions, but we did not detect selection among 20 PLVA isolates from bobcats. These findings support the hypothesis that PLVA is a bobcat-adapted virus which is less fit in mountain lions and under intense selection pressure in the novel host. Ancestral reconstruction of transmission events reveals that intraspecific PLVA transmission has occurred among panthers () in Florida following the initial cross-species infection from bobcats. In contrast, interspecific transmission from bobcats to mountain lions predominates in California. These findings document outcomes of cross-species lentiviral transmission events among felids that compare to the emergence of HIV from nonhuman primates. Cross-species transmission episodes can be singular, dead-end events or can result in viral replication and spread in the new species. The factors that determine which outcome will occur are complex, and the risk of new virus emergence is therefore difficult to predict. We used molecular techniques to evaluate the transmission, fitness, and adaptation of puma lentivirus A (PLVA) between bobcats and mountain lions in two geographic regions. Our findings illustrate that mountain lion exposure to PLVA is relatively common but does not routinely result in communicable infections in the new host. This is attributed to efficient species barriers that largely prevent lentiviral adaptation. However, the evolutionary capacity for lentiviruses to adapt to novel environments may ultimately overcome host restriction mechanisms over time and under certain ecological circumstances. This phenomenon provides a unique opportunity to examine cross-species transmission events leading to new lentiviral emergence.
由于宿主 - 寄生虫共同进化的复杂历史，慢病毒表现出高度的物种特异性。鉴于人类免疫缺陷病毒（HIV）在人类接触猿猴免疫缺陷病毒（SIV）后出现的病毒考古学记录详尽，了解促进成功跨物种慢病毒传播的过程具有高度相关性。我们之前报道过在加利福尼亚州和佛罗里达州的少数动物中，一种猫免疫缺陷病毒亚型——美洲狮慢病毒A（PLVA）在短尾猫和美洲狮之间发生了自然跨物种传播。在本研究中，我们调查了来自自由放养短尾猫和美洲狮的大量PLV分离株中的宿主特异性选择压力、宿主体内病毒适应性以及种间与种内传播模式。对前病毒和病毒RNA水平的分析表明，与短尾猫相比，PLVA在美洲狮中的适应性受到严重限制。我们记录了来自美洲狮的六个PLVA基因组中有三个存在多样化选择的证据，但在来自短尾猫的20个PLVA分离株中未检测到选择。这些发现支持了这样的假设，即PLVA是一种适应短尾猫的病毒，在美洲狮中适应性较差，且在新宿主中面临强烈的选择压力。对传播事件的祖先重建表明，在最初从短尾猫发生跨物种感染后，佛罗里达州的美洲豹之间发生了PLVA的种内传播。相比之下，在加利福尼亚州，从短尾猫到美洲狮的种间传播占主导。这些发现记录了猫科动物之间跨物种慢病毒传播事件的结果，可与HIV从非人灵长类动物中出现的情况相比较。跨物种传播事件可能是单一的、无后续传播的事件，也可能导致病毒在新物种中复制和传播。决定会出现哪种结果的因素很复杂，因此新病毒出现的风险难以预测。我们使用分子技术评估了美洲狮慢病毒A（PLVA）在两个地理区域的短尾猫和美洲狮之间的传播、适应性和适应性。我们的研究结果表明，美洲狮接触PLVA相对常见，但通常不会在新宿主中导致可传播的感染。这归因于有效阻止慢病毒适应的物种屏障。然而，随着时间的推移以及在某些生态情况下，慢病毒适应新环境的进化能力最终可能会克服宿主限制机制。这种现象为研究导致新慢病毒出现的跨物种传播事件提供了独特的机会。
