Ghaly Timothy M, Focardi Amaranta, Elbourne Liam D H, Sutcliffe Brodie, Humphreys William F, Jaschke Paul R, Tetu Sasha G, Paulsen Ian T
School of Natural Sciences, Macquarie University, Sydney, Australia.
Climate Change Cluster (C3), University of Technology Sydney, Sydney, Australia.
Environ Microbiome. 2024 Jan 30;19(1):9. doi: 10.1186/s40793-024-00549-6.
Viruses play important roles in modulating microbial communities and influencing global biogeochemistry. There is now growing interest in characterising their ecological roles across diverse biomes. However, little is known about viral ecology in low-nutrient, chemotrophic-based environments. In such ecosystems, virus-driven manipulation of nutrient cycles might have profound impacts across trophic levels. In particular, anchialine environments, which are low-energy underground estuaries sustained by chemotrophic processes, represent ideal model systems to study novel virus-host-environment interactions.
Here, we employ metagenomic sequencing to investigate the viral community in Bundera Sinkhole, an anchialine ecosystem rich in endemic species supported by microbial chemosynthesis. We find that the viruses are highly novel, with less than 2% representing described viruses, and are hugely abundant, making up as much as 12% of microbial intracellular DNA. These highly abundant viruses largely infect important prokaryotic taxa that drive key metabolic processes in the sinkhole. Further, the abundance of viral auxiliary metabolic genes (AMGs) involved in nucleotide and protein synthesis was strongly correlated with declines in environmental phosphate and sulphate concentrations. These AMGs encoded key enzymes needed to produce sulphur-containing amino acids, and phosphorus metabolic enzymes involved in purine and pyrimidine nucleotide synthesis. We hypothesise that this correlation is either due to selection of these AMGs under low phosphate and sulphate concentrations, highlighting the dynamic interactions between viruses, their hosts, and the environment; or, that these AMGs are driving increased viral nucleotide and protein synthesis via manipulation of host phosphorus and sulphur metabolism, consequently driving nutrient depletion in the surrounding water.
This study represents the first metagenomic investigation of viruses in anchialine ecosystems, and provides new hypotheses and insights into virus-host-environment interactions in such 'dark', low-energy environments. This is particularly important since anchialine ecosystems are characterised by diverse endemic species, both in their microbial and faunal assemblages, which are primarily supported by microbial chemosynthesis. Thus, virus-host-environment interactions could have profound effects cascading through all trophic levels.
病毒在调节微生物群落和影响全球生物地球化学方面发挥着重要作用。目前，人们对其在不同生物群落中的生态作用的研究兴趣日益浓厚。然而，对于低营养、基于化学合成的环境中的病毒生态学却知之甚少。在这样的生态系统中，病毒驱动的营养循环操纵可能会对各个营养级产生深远影响。特别是，咸淡水环境是由化学合成过程维持的低能量地下河口，是研究新型病毒-宿主-环境相互作用的理想模型系统。
在这里，我们采用宏基因组测序来研究邦德拉落水洞的病毒群落，这是一个由微生物化学合成支持的、富含特有物种的咸淡水生态系统。我们发现这些病毒非常新颖，只有不到2%的病毒与已知病毒相似，而且数量极其丰富，占微生物细胞内DNA的比例高达12%。这些高度丰富的病毒主要感染驱动落水洞关键代谢过程的重要原核生物类群。此外，参与核苷酸和蛋白质合成的病毒辅助代谢基因（AMGs）的丰度与环境中磷酸盐和硫酸盐浓度的下降密切相关。这些AMGs编码了生产含硫氨基酸所需的关键酶，以及参与嘌呤和嘧啶核苷酸合成的磷代谢酶。我们推测，这种相关性要么是由于在低磷酸盐和硫酸盐浓度下对这些AMGs的选择，突出了病毒、其宿主和环境之间的动态相互作用；要么是这些AMGs通过操纵宿主的磷和硫代谢来促进病毒核苷酸和蛋白质的合成增加，从而导致周围水体中的营养物质消耗。
本研究是对咸淡水生态系统中病毒的首次宏基因组研究，并为这种“黑暗”,低能量环境中的病毒-宿主-环境相互作用提供了新的假设和见解。这一点尤为重要，因为咸淡水生态系统的特点是在微生物和动物群落中都有多样的特有物种，而这些主要由微生物化学合成来维持。因此，病毒-宿主-环境相互作用可能会对所有营养级产生深远的连锁反应。
