Ecophysiological and genomic analyses of a representative isolate of highly abundant <scp><i>Bacillus cereus</i></scp> strains in contaminated subsurface sediments

Goff, Jennifer; Szink, Elizabeth G; Thorgersen, Michael P.; Putt, Andrew D.; Fan, Yuhang; Lui, Lauren M.; Nielsen, Torben; Hunt, Kristopher A.; Michael, Jonathan P.; Wang, Yajiao; Ning, Daliang; Fu, Ying; Nostrand, Joy D. Van; Poole, Farris L.; Chandonia, John-Marc; Hazen, Terry C.; Stahl, David A.; Zhou, Jizhong; Arkin, Adam P.; Adams, Michael W. W.

doi:10.1111/1462-2920.16173

Cited by 7 publications

(20 citation statements)

References 101 publications

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“…Nitrite accumulation has been measured in the porewaters of contaminated ORR sediment cores, suggestive of inhibition of nitrite reduction in situ [ 75 ]. Strain CPTF carries out DNRA via the NarGHI respiratory nitrate reductase and NasDE nitrite reductase [ 30 ]. Both NarGHI and NasDE contain iron cofactors [ 76 , 77 ].…”

Section: Resultsmentioning

confidence: 99%

“…Bacillus cereus str. CPT56D-587-MTF (referred to as strain CPTF) [ 30 , 31 ] was routinely streaked out on LB plates and grown overnight at 30 °C. A single isolated colony was inoculated into LB broth and grown overnight shaking at 200 rpm at 30 °C.…”

Section: Methodsmentioning

confidence: 99%

“…Strain CPTF carries out dissimilatory nitrate reduction to ammonium (DNRA) via NarGHI and NasDE [ 30 ] and is a representative isolate of a highly abundant amplicon sequence variant (ASV) found in the subsurface sediments of Area 3. In a recent study, this CPTF-matching ASV had the highest relative abundance across all Area 3 samples, up to 10–40% of total reads in several samples, suggesting that strain CPTF represents a dominant species in this region [ 30 ]. Thus, this isolate is ideal for detailed studies of physiological responses to site-relevant stressors.…”

Section: Introductionmentioning

confidence: 99%

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Mixed heavy metal stress induces global iron starvation response

et al. 2022

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Multiple heavy metal contamination is an increasingly common global problem. Heavy metals have the potential to disrupt microbially mediated biogeochemical cycling. However, systems-level studies on the effects of combinations of heavy metals on bacteria are lacking. For this study, we focused on the Oak Ridge Reservation (ORR; Oak Ridge, TN, USA) subsurface which is contaminated with several heavy metals and high concentrations of nitrate. Using a native Bacillus cereus isolate that represents a dominant species at this site, we assessed the combined impact of eight metal contaminants, all at site-relevant concentrations, on cell processes through an integrated multi-omics approach that included discovery proteomics, targeted metabolomics, and targeted gene-expression profiling. The combination of eight metals impacted cell physiology in a manner that could not have been predicted from summing phenotypic responses to the individual metals. Exposure to the metal mixture elicited a global iron starvation response not observed during individual metal exposures. This disruption of iron homeostasis resulted in decreased activity of the iron-cofactor-containing nitrate and nitrite reductases, both of which are important in biological nitrate removal at the site. We propose that the combinatorial effects of simultaneous exposure to multiple heavy metals is an underappreciated yet significant form of cell stress in the environment with the potential to disrupt global nutrient cycles and to impede bioremediation efforts at mixed waste sites. Our work underscores the need to shift from single- to multi-metal studies for assessing and predicting the impacts of complex contaminants on microbial systems.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mixed heavy metal stress induces global iron starvation response

et al. 2022

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“…Previously, we isolated Bacillus cereus strain CPT56D-587-MTF (referred to as strain CPTF) from the subsurface sediments of the ORR Area 3. Strain CPTF carries out dissimilatory nitrate reduction to ammonium via NarGHI and NasDE [29]. Importantly, strain CPTF is a representative isolate of a highly abundant amplicon sequence variant (ASV) found in the Area 3 subsurface sediments.…”

Section: Introductionmentioning

confidence: 99%

“…Importantly, strain CPTF is a representative isolate of a highly abundant amplicon sequence variant (ASV) found in the Area 3 subsurface sediments. In a recent sediment survey, this ASV had the highest relative abundance across all Area 3 sediment samples with an abundance up to 10-40% of total reads in several samples, suggesting that strain CPTF represents a dominant taxon at the site [29]. Thus, this isolate is ideal for detailed studies of the physiological responses of native microbiota to site-relevant stressors.…”

Section: Introductionmentioning

confidence: 99%

Mixed Heavy Metals Stress Induces Global Iron Starvation as Revealed by System Level Multi-Omic Analyses

Goff

Chen

Thorgersen

et al. 2022

Preprint

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Globally, multiple heavy metal contamination is an increasingly common problem. As heavy metals have the potential to disrupt microbially-mediated biogeochemical cycling, it is critical to understand their impact on microbial physiology. However, systems-level studies on the effects of a combination of heavy metals on bacteria are lacking. Here, we use a native Bacillus cereus isolate from the subsurface of the Oak Ridge Reservation (ORR; Oak Ridge, TN, USA)- representing a highly abundant species at the site - to assess the combined impact of eight metal contaminants. Using this metal mixture and individual metals, all at concentrations based on the ORR site geochemistry, we performed growth experiments and proteomic analyses of the B. cereus strain, in combination with targeted MS-based metabolomics and gene expression profiling. The combination of eight metals impacts cell physiology in a manner that could not have been predicted from summing phenotypic responses to the individual metals. Specifically, exposure to the metal mixture elicited global iron starvation responses not observed in any of the individual metal treatments. As nitrate is also a significant contaminant at the ORR site and nitrate and nitrite reductases are iron-containing enzymes, we also examined the effects of the metal mixture on reduction of nitrogen oxides. We found that the metal mixture inhibits the activity of these enzymes through a combination of direct enzymatic damage and post-transcriptional and post-translational regulation. Altogether, these data suggest that metal mixture studies are critical for understanding how multiple rather than individual metals influence microbial processes in the environment.

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Mixed waste contamination selects for a mobile genetic element population enriched in multiple heavy metal resistance genes

Goff,

Lui,

Nielsen

et al. 2024

ISME Communications

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Mobile genetic elements (MGEs) like plasmids, viruses, and transposable elements can provide fitness benefits to their hosts for survival in the presence of environmental stressors. Heavy metal resistance genes (HMRGs) are frequently observed on MGEs, suggesting that MGEs may be an important driver of adaptive evolution in environments contaminated with heavy metals. Here, we report the meta-mobilome of the heavy metal-contaminated regions of the Oak Ridge Reservation (ORR) subsurface. This meta-mobilome was compared to one derived from samples collected from unimpacted regions of the ORR subsurface. We assembled 1615 unique circularized DNA elements that we propose to be MGEs. The circular elements from the highly contaminated subsurface were enriched in HMRG clusters relative to those from the nearby unimpacted regions. Additionally, we found that these HMRGs were associated with Gamma and Betaproteobacteria hosts in the contaminated subsurface and potentially facilitate the persistence and dominance of these taxa in this region. Finally, the HMRGs were associated with conjugative elements, suggesting their potential for future lateral transfer. We demonstrate how our understanding of MGE ecology, evolution, and function can be enhanced through the genomic context provided by completed MGE assemblies.

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Ecophysiological and genomic analyses of a representative isolate of highly abundant Bacillus cereus strains in contaminated subsurface sediments

Cited by 7 publications

References 101 publications

Mixed heavy metal stress induces global iron starvation response

Mixed heavy metal stress induces global iron starvation response

Mixed Heavy Metals Stress Induces Global Iron Starvation as Revealed by System Level Multi-Omic Analyses

Mixed waste contamination selects for a mobile genetic element population enriched in multiple heavy metal resistance genes

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