Host-microbe symbioses are an essential component of many ecological systems, playing critical roles in the physiology and evolution of all involved partners. In this context, the bacterial family that includes Coxiella burnetii, the causative agent of Q fever, is of particular interest. The Coxiellaceae family is a complex group with members that have adopted a variety of specializations. Closely related lineages to C. burnetii are tick mutualists (Coxiella-like endosymbionts) and aquatic bacteria that may include both free living and symbiotic species. Additionally, four related genera within this family include symbionts of insects and amoebae. Exactly how and when pathogenicity and mutualism evolved in this lineage is not clear, thus remaining a valuable line of enquiry that can help establish general principles on these lifestyle transitions.

A new study by Santos-Garcia and colleagues (2023) places the spotlight on this bacterial group, obtaining new insights through comparative genomics. The authors add two genomes, one of them a circular contig representing a highly reduced (0.9 Mb) chromosome, that increase the resolution of key branches in the Coxiella evolutionary tree. These include a sister group to C. burnetii and the group immediately subtending them, both entirely containing Coxiella-like endosymbionts. By analyzing genetic potential for metabolism, cell dimorphism, virulence and acidophily, the authors find evidence for the ancestrality of genes associated with a pathogenic lifestyle, and support a scenario by which mutualism arose multiple times in a parasitic lineage. In this context shines a pathogenicity island acquired in the common ancestor of this group and subsequently eroded in mutualistic lineages. This scenario highlights the importance of pre-adaptations that facilitate evolutionary specializations, such as the capabilities for B vitamin biosynthesis (key feature in the adaptation to a mutualistic relationship with organisms with B-vitamin-poor diets) and pH homeostasis (harnessed by C. burnetii for infection). 

Microbial groups at the crossroads of parasitism and mutualism help us understand the mechanisms underpinning these evolutionary strategies (see e.g. Drew et al, 2021). Transitions in endosymbiosis, including shifts in the parasitism-mutualism continuum, adaptation to new partners, or switches between free-living and host-associated lifestyles, affect the structure of ecological networks, and understanding them can yield crucial insights into how to manipulate microbial symbioses for health outcomes, sustainable agriculture or ecosystem conservation. The Coxiellaceae, by including a diverse set of mutualistic, parasitic and possibly free-living lineages, are a fantastic model group to tackle these questions. Together with other host-associated bacteria, such as Sodalis (Clayton et al, 2012) or Pantoea (Walterson and Stavrinides, 2015) species, these ecologically diverse microbes are valuable assets in the quest to decipher the molecular basis of lifestyle transitions in endosymbiosis.

REFERENCES

Clayton, A.L., et al (2012). A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect–bacterial symbioses. PLoS Genetics, 8: e1002990. https://doi.org/10.1371/journal.pgen.1002990

Drew, G.C., Stevens, E.J., King, K.C. (2021). Microbial evolution and transitions along the parasite-mutualist continuum. Nature Reviews Microbiology, 19: 623-638. https://doi.org/10.1038/s41579-021-00550-7

Santos-Garcia, D., et al. (2023) Genomic changes during the evolution of the Coxiella genus along the parasitism-mutualism continuum. bioRxiv, 2022.10.26.513839, ver. 4 peer-reviewed and recommended by Peer Community In Microbiology. https://doi.org/10.1101/2022.10.26.513839

Walterson, A.M., Stavrinides, J. (2015). Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiology Reviews, 39: 968-984. https://doi.org/10.1093/femsre/fuv027

Plant pathogens can cause devastating damage to crop (Strange and Scott 2005) greatly affecting a food resource in growing need on our planet. A significant proportion of global crops require irrigation, and with this, bare the risk of being affected by irrigation-borne pathogens (Lamichhane and Bartoli, 2015). Detection of plant pathogens in irrigation water can effectively be used to minimize this risk. River water makes up a major irrigation water source. Morris et al., (2023), propose monitoring whole river catchments to understand plant pathogen population dynamics and generate models to prevent outbreaks, similar to practices regarding water-borne human pathogens.

Monitoring 270 km of the river Durance, Morris et al., (2023) reveal that two groups of bacteria known to host pathogenic strains, Pseudomonas syringae and the Soft Rot Pectobacteriaceae are present in relatively high numbers across the entire catchment or significant parts of it, respectively, with their abundance mostly correlated to water temperature. Nevertheless, despite their presence no major outbreaks have been reported in recent years. The authors suggest that the current environmental conditions in the lower, agriculture-dominated part of the catchment may not generate the necessary environment for an outbreak. Alternatively, as also suggested, though some potentially pathogenic variants were detected in the study, they may not match the crops currently grown in the area (Morris et al., 2023).

The authors thus bring up the need for large scale monitoring and call for observations on potential land-use changes in the area that may alter the sensitive and seemingly stable conditions in such a way that outbreaks will be triggered. Change of land use, specifically from rural to agricultural use, has been repeatedly recognized to influence biodiversity (e.g., Ionescu et al., 2022). Furthermore, agricultural environments, with a dense network of irrigation channels, natural and man-made ponds, and larger reservoirs, will accelerate the spread of organisms through multiple biotic and abiotic vectors (Karnatak and Wollrab, 2020), and with this likely plant- (and other) pathogens. Overall, the work by Morris et al., (2023) highlights that studying the presence and distribution of plant pathogens in water used for irrigation across large areas, is bound to identify which potential pathogens are omnipresent, awaiting for the right condition for an outbreak; and which are rather spread from, isolated, local sources and thus can be effectively mitigated.

References

Strange, R. N., and Scott, P. R. (2005). Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43, 83–116. https://doi.org/10.1146/annurev.phyto.43.113004.133839

Lamichhane, J.R. and Bartoli, C. (2015), Plant pathogenic bacteria in open irrigation systems: what risk for crop health? Plant Pathol, 64: 757-766. https://doi.org/10.1111/ppa.12371

C.E. Morris, C. Lacroix, C. Chandeysson, C. Guilbaud, C. Monteil, S. Piry, Rochelle Newall E., S. Fiorini, F. Van Gijsegem, M.A. Barny, O. Berge (2023) Comparative abundance and diversity of populations of the Pseudomonas syringae and Soft Rot Pectobacteriaceae species complexes throughout the Durance River catchment from its French Alps sources to its delta. bioRxiv, 2022.09.06.506731, ver. 3 peer-reviewed and recommended by Peer Community in Microbiology. https://doi.org/10.1101/2022.09.06.506731 

Ionescu, D., Bizic, M., Karnatak, R., Musseau, C. L., Onandia, G., Kasada, M., Berger, S. A., et al. (2022). From Microbes to Mammals: Pond Biodiversity Homogenization across Different Land-Use Types in an Agricultural Landscape. Ecological Monographs 92(3): e1523. https://doi.org/10.1002/ecm.1523

Engineering plant microbiota can improve plant health and growth sustainably. Emergent approaches include rational Synthetic Communities (SynCom) design or soil amendments and specific agricultural practices to shift resident microbiota and to understand its impact (Moreira et al. 2023). 

In this context, the impact of seed microbiota on the early stages of plant development is becoming an essential topic in the study of plant–microbiota interactions. Behind the well-studied seed-borne pathogens, the seed microbiota can host many other commensal and beneficial organisms that have been neglected in the past. 

The study of Simonin et al. (2023) applies single isolates and synthetic communities (SynCom)  on radish seeds to answer two key questions: what is the role of seed microbiota during the early stages of plant development? How can SynCom influence the seedling health and its microbiota? The study describes an elegant approach to cope with the variability of natural microbiota using SynCom following a gradient of complexity. 

Overall, the study highlighted a contrasted impact of the bacterial strains when applied in isolation or SynCom. The composition and complexity of the SynCom had also an impact on plant seedlings. Importantly, contrasting evolution from seeds to seedlings was observed for 3 strains of Pseudomonas fluorescens within the SynComs, underlining the importance of intra-species level diversity and precluding any generalization of results at species level.  

References 

Moreira, Z. P. M., Chen, M. Y., Ortuno, D. L. Y., & Haney, C. H. (2023). Engineering plant microbiomes by integrating eco-evolutionary principles into current strategies. Current Opinion in Plant Biology, 71, 102316. https://doi.org/10.1016/j.pbi.2022.102316

Simonin, M., Préveaux, A., Marais, C., Garin, T., Arnault, G., Sarniguet, A., & Barret, M. (2023). Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype. bioRxiv, 2023-02. ver. 3 peer-reviewed and recommended by Peer Community in Microbiology. https://doi.org/10.1101/2023.02.14.527860

ONT long-read high-throughput sequencing is not routinely used for metabarcoding studies of microbial communities. Even though this technology is supposed to considerably improve phylogenetic coverage and taxonomic resolution, it initially suffered from relatively poor read accuracy.  Assessment of the performance of this new approach in comparison with routinely used 16S rDNA short-read sequencing is therefore needed to validate its use.

The study by Lemoinne et al. (2023) offers a comprehensive comparison of two 16S rDNA metabarcoding approaches on marine sediment samples. By comparing Illumina short-read sequencing with ONT long-read sequencing, the authors conclude that bacterial community structures inferred from both technologies were similar. They also found that differences observed between sampling sites and along the sea-land orientation were comparable between the two technologies. However, the choice of technology still has an impact on the obtained results, notably in terms of bacterial diversity retrieved, taxonomic resolution, and replicability between biological replicates.

Altogether, these results validate the use of ONT long-read sequencing for 16S metabarcoding approaches in marine sediments. Comparisons of such kinds targeting other remote environments are needed, as they might offer new opportunities for field scientists with no access to sequencing platforms to study the structure and composition of microbial communities.

Reference

Lemoinne, A., Dirberg, G., Georges, M., & Robinet, T. (2023). Fine-scale congruence in bacterial community structure from marine sediments sequenced by short-reads on Illumina and long-reads on Nanopore. biorXiv, version 3 peer-reviewed and recommended by Peer Community in Microbiology. https://doi.org/10.1101/2023.06.06.541006

Shrimp aquaculture ponds are an established technology that helps answer the demand for high-protein food while reducing the impact of fishing on the oceans.

However, as a closed system, high in organic matter, aquaculture ponds in general and those used for shrimp in particular tend to develop anoxic sediments and favour sulfate reduction to H2S. The development of hydrogen sulphide, in return, is toxic to the shrimp and can lead to lower yields.

A standard solution to the problem is to inject air into the sediments. However, this solution requires additional infrastructure, is costly to operate, and can also disturb other essential life forms in the pond, such as benthic plants. 

In this work by Torun et al. (2024), the authors used a carefully designed lab model of shrimp ponds to show that the addition of molybdate at concentrations as low as 5 mg/l delayed the accumulation of H2S and pushed the zone rich in sulphide deeper into the sediment.

The postulated mechanism for the inhibition in H2S production is that molybdate binds to the ATP sulfurylase in sulphate-reducing bacteria (SRB), and together with ATP, they generate adenosine 5′-phosphosulfate (APS) that cannot be used as an electron acceptor.

Surprisingly, however, the growth of SRB was stimulated rather than inhibited in this experiment. While the exact cause remains unknown, the authors postulate that SRB resorted to alternative metabolic pathways such as fermentation.

Overall, while this work was done on a model system in the lab, adding molybdate to shrimp aquaculture ponds is a promising technique and should be tested on a larger scale.

Reference

Torun F, Hostins B, Schryver PD, Boon N, Vrieze JD. (2024). Molybdate delays sulphide formation in the sediment and transfer to the bulk liquid in a model shrimp pond. bioRxiv, ver.3, peer-reviewed and recommended by Peer Community In Microbiology. https://doi.org/10.1101/2023.11.16.567380