When we think of Listeria monocytogenes, we usually think of contaminated food and the severe threat it poses to vulnerable populations like children, the elderly, pregnant women, and the immunocompromised. But long before this germ reaches our plates, it lives in the soil beneath our feet. L. monocytogenes is divided into four evolutionary lineages (aka family groups), three of which are widely found in soils. Until now, exactly how these bacteria adapt and survive in their natural soil reservoirs has remained a mystery. In our recent study using our United State-wide Listeria collection (Liao et al., Nat Microbiol, 2021), we uncovered how the soil environment shapes the pathogen's genetic variability, potentially influencing its ability to persist, spread through environmental pathways, and contribute to human outbreaks.
To understand how L. monocytogenes adapts, we first explored how non-living (i.e., abiotic) factors such as climate and soil chemistry influence its genetic variation. We found that precipitation and soil elements like pH, aluminum, and molybdenum (an essential inorganic ion for biochemical processes) act as important evolutionary pressures. For instance, alternating wet and dry weather cycles subject the bacteria to severe dehydration and osmotic stress. Shifts in soil pH directly impact the bioavailability of elements like aluminum and molybdenum. To survive these harsh conditions, L. monocytogenes can gain or lose genes to modify its protective outer layer (i.e., the cell envelope) and bolster its internal defense mechanisms.
But L. monocytogenes does not live in isolation; it shares the soil with a bustling microscopic neighborhood of other bacteria. Our study revealed that these living (i.e., biotic) factors are just as critical to the pathogen's evolution. We found that the presence of specific bacterial groups, such as Nitrospirae, is strongly associated with differences in the genetic makeup of L. monocytogenes populations. Nitrospirae play important roles in nitrogen cycling and are associated with environments where reactive nitrogen compounds, including nitrite, can accumulate. Because nitrite can inhibit L. monocytogenes growth, interactions with Nitrospirae may create selective pressures on the pathogen. To cope with hostile neighbors like these, the pathogen may adapt its survival strategies, specifically by modifying its protective outer layer and its DNA repair mechanisms.
When we look closer, we observe striking differences in genomic flexibility (i.e., the ability to gain, lose, or reorganize genes) across L. monocytogenes family groups, which also occupy distinct ecological niches. Much of this variation is associated with genes responsible for building their protective outer layer. We also found that lineage I appears to have a larger individual genome size compared to lineage III. However, the pangenome (i.e., the collective genetic toolkit) of lineage III is much more 'open,' meaning its members can more readily acquire or lose genes in response to local environmental pressures. This adaptability may help explain why lineage III frequently co-occurs with Nitrospirae, which are commonly found in nutrient-poor environments. These findings suggest that lineage III is capable of living in harsh, nutrient-limited soils, possibly benefiting from its more streamlined genomic strategy that reduces the costs of maintaining unnecessary genes.
While lineage III behaves more like a homebody, adapting to local conditions, lineage I behaves more like a frequent traveler. We found that lineage I spread widely across geographic regions, such as from the East to the West of U.S., allowing populations from distant locations (up to 4,000 km apart!) to remain genetically similar. This travel habit, potentially aided by the food transport chain, has profound implications for public health. Because lineage I appears to disperse more widely, it may have a greater opportunity to move from natural soils into agricultural fields and food processing facilities. From there, it can easily reach our plates through contaminated produce. In fact, when we compared our soil data with clinical samples, we found genomic evidence linking soil-derived lineage I isolates to strains recovered from human infections.
TL;DR
- Climate, soil chemistry, and neighboring microbes may all influence how monocytogenes adapts and survives in the environment.
- monocytogenes lineages show differences in genomic flexibility and occupy distinct ecological niches.
- Lineage I appears more capable of spreading across landscapes and may have a greater potential to contribute to foodborne outbreak.
The takeaway is clear: We cannot treat all L. monocytogenes as a single, uniform threat. To protect our food supply, we need tailored, lineage-specific monitoring in natural environments near farms. By tracking L. monocytogenes lineages, we may be better able to predict their movement and improve efforts to prevent foodborne outbreaks.
Reference
Liao, J., Guo, X., Weller, D.L. et al. Nationwide genomic atlas of soil-dwelling Listeria reveals effects of selection and population ecology on pangenome evolution. Nat Microbiol 6, 1021–1030 (2021). https://doi.org/10.1038/s41564-021-00935-7
Acknowledgement
We would like to thank Carrie Kroehler from the Center for Communicating Science at Virginia Tech for her helpful comments and suggestions to improve this article.