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Spero, M. A.

Publications and source records attributed to Spero, M. A..

3 recordsLinked to original sources

New genetic tools in Finegoldia magna identify a conserved adhesin required for the formation of stress-tolerant aggregates

The Gram-positive obligate anaerobe Finegoldia magna is a member of the healthy human microbiota, but also acts as an opportunistic pathogen to cause persistent, biofilm-associated infections. Despite its prevalence on the human host, little is known about F. magna biology or the mechanisms underlying its clinically relevant phenotypes, partly due to the lack of genetic tools. We address this gap by establishing genetic approaches for investigating gene function in F. magna, which we apply to identify genetic determinants of aggregate biofilm formation. We found that F. magna isolates are naturally competent, allowing for targeted chromosomal integration of linear DNA constructs via homologous recombination. Transformation frequency varied substantially among strains and was also affected by factors such as homologous flank length, DNA concentration, and incubation method. To identify genes that mediate aggregate biofilm formation, we used experimental evolution to select for F. magna mutants that had lost the ability to aggregate. This approach identified a conserved locus encoding a putative adhesin that we named FafA (Finegoldia adhesion factor A). Next, we applied targeted mutagenesis tools to show that deletion of fafA markedly reduced autoaggregation but does not impair other modes of biofilm formation, including surface attachment or aggregation during agitation. Finally, we demonstrate that FafA-mediated aggregation protects F. magna from antibiotic and oxidative stress. Together, these findings establish a genetic framework for mechanistic studies in F. magna and identify FafA as a conserved adhesin that promotes aggregation and stress tolerance in this anaerobic pathobiont.

microbiology↗

Host nutrients drive paired-substrate growth and distinct biofilm lifestyles in Finegoldia magna

Host-associated bacteria navigate complex nutrient landscapes where metabolites act as both growth substrates and cues that shape behavior. Yet, for most commensal and pathogenic bacteria, the nutrients and metabolisms that support persistence in the host remain unknown. Finegoldia magna is an obligate anaerobe that normally colonizes human skin and mucosal surfaces but also causes persistent biofilm-associated infections on implanted medical devices and in chronic wounds. Here, we developed a defined medium to investigate how nutrients influence F. magna physiology. We found that F. magna has a remarkably restricted metabolism that is specialized to use a limited set of host-relevant nutrients, including glycine, fructose, nucleosides, and betaine. Carbon-source screens showed glycine was the only substrate that supported growth as a sole carbon source. Instead, growth typically required two carbon substrates: a compatible electron donor-acceptor pair, suggesting redox balance imposes major constraints on its metabolism. To determine whether these constraints extend to host environments, we cultured F. magna in media derived from human chronic wound tissue. Despite its chemical complexity, F. magna displayed a similarly restricted metabolic profile, primarily consuming peptides, nucleosides, and betaine. These nutrients also directed biofilm behavior, with different metabolites promoting surface attachment or aggregation. Our findings show that although F. magna lacks metabolic flexibility, this opportunistic pathogen appears specialized to exploit host-derived products of skin physiology, tissue damage, and inflammation. This work suggests that host-associated bacteria with highly specialized metabolisms may be especially responsive to nutrient availability, linking local metabolite composition to key persistence behaviors like biofilm formation.

microbiology↗

Visualization of mRNA Expression in Pseudomonas aeruginosa Aggregates Reveals Spatial Patterns of Fermentative and Denitrifying Metabolism

Gaining insight into the behavior of bacteria at the single cell level is important given that heterogeneous microenvironments strongly influence microbial physiology. The hybridization chain reaction (HCR) is a technique that provides in situ molecular signal amplification, enabling simultaneous mapping of multiple target RNAs at small spatial scales. To refine this method for biofilm applications, we designed and validated new probes to visualize expression of key catabolic genes in Pseudomonas aeruginosa aggregates. In addition to using existing probes for the dissimilatory nitrate reductase (narG), we developed probes for a terminal oxidase (ccoN1), nitrite reductase (nirS), nitrous oxide reductase (nosZ), and acetate kinase (ackA). These probes can be used to determine gene expression levels both in liquid culture and in biofilms. Using these probes, we quantified gene expression across oxygen gradients in aggregate populations grown using the agar block biofilm assay (ABBA). We observed distinct patterns of catabolic gene expression, with upregulation occurring in particular ABBA regions both within individual aggregates and over the aggregate population. Aerobic respiration (ccoN1) showed peak expression under oxic conditions, whereas fermentation (ackA) showed peak expression in the anoxic cores of high metabolic activity aggregates near the air-agar interface. Denitrification genes narG, nirS, and nosZ showed peak expression in hypoxic and anoxic regions, although nirS expression was much stronger in anoxic environments compared to other denitrification genes. These results reveal that the microenvironment correlates with catabolic gene expression in aggregates, and demonstrate the utility of HCR in unveiling cellular activities at the microscale in heterogeneous populations. ImportanceTo understand bacteria in diverse contexts we must understand the variations in behaviors and metabolisms they express spatiotemporally. Populations of bacteria are known to be heterogeneous, but the ways this variation manifests can be challenging to characterize due to technical limitations. By focusing on energy conservation, we demonstrate that HCR v3.0 can visualize nuances in gene expression, allowing us to understand how metabolism in Pseudomonas aeruginosa biofilms responds to microenvironmental variation at high spatial resolution. We validated probes for four catabolic genes: a constitutively expressed oxidase, acetate kinase, nitrite reductase, and nitrous oxide reductase. We showed that the genes for different modes of metabolism are expressed in overlapping but distinct subpopulations according to oxygen concentrations in a predictable fashion. The spatial transcriptomic technique described here has the potential to be used to map microbial activities across diverse environments.

microbiology↗