Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole

Qian Xiang; Hryhoriy Stryhanyuk; Matthias Schmidt; Steffen Kümmel; Hans H. Richnow; Yong Guan Zhu; Li Cui; Niculina Musat

doi:10.1016/j.envpol.2024.124197

Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole

Qian Xiang, Hryhoriy Stryhanyuk, Matthias Schmidt, Steffen Kümmel, Hans H. Richnow, Yong Guan Zhu, Li Cui, Niculina Musat^*

^*Corresponding author for this work

Department of Biology - Microbiology

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

1 Citation (Scopus)

Abstract

The presence and accumulation of both, plastics and antibiotics in soils may lead to the colonization, selection, and propagation of soil bacteria with certain metabolic traits, e.g., antibiotic resistance, in the plastisphere. However, the impact of plastic-antibiotic tandem on the soil ecosystem functioning, particularly on microbial function and metabolism remains currently unexplored. Herein, we investigated the competence of soil bacteria to colonize plastics and degrade ¹³C-labeled sulfamethoxazole (SMX). Using single-cell imaging, isotope tracers, soil respiration and SMX mineralization bulk measurements we show that microbial colonization of polyethylene (PE) and polystyrene (PS) surfaces takes place within the first 30 days of incubation. Morphologically diverse microorganisms were colonizing both plastic types, with a slight preference for PE substrate. CARD-FISH bacterial cell counts on PE and PS surfaces formed under SMX amendment ranged from 5.36 × 10³ to 2.06 × 10⁴, and 2.06 × 10³ to 3.43 × 10³ hybridized cells mm⁻², respectively. Nano-scale Secondary Ion Mass Spectrometry measurements show that ¹³C enrichment was highest at 130 days with values up to 1.29 atom%, similar to those of the ¹³CO₂ pool (up to 1.26 atom%, or 22.55 ‰). Independent Mann-Whitney U test showed a significant difference between the control plastisphere samples incubated without SMX and those in ¹³C-SMX incubations (P < 0.001). Our results provide direct evidence demonstrating, at single-cell level, the capacity of bacterial colonizers of plastics to assimilate ¹³C-SMX from contaminated soils. These findings expand our knowledge on the role of soil-seeded plastisphere microbiota in the ecological functioning of soils impacted by anthropogenic stressors.

Original language	English
Article number	124197
Journal	Environmental Pollution
Volume	355
Number of pages	10
ISSN	0269-7491
DOIs	https://doi.org/10.1016/j.envpol.2024.124197
Publication status	Published - Aug 2024

Keywords

Antibiotics
Biofilm formation
FISH-SIP-nanoSIMS
Plastics
Single-cell imaging
Sulfamethoxazole degradation

Access to Document

10.1016/j.envpol.2024.124197

Cite this

@article{6b9e8bb329044c1aa3b7a583fdba7194,

title = "Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole",

abstract = "The presence and accumulation of both, plastics and antibiotics in soils may lead to the colonization, selection, and propagation of soil bacteria with certain metabolic traits, e.g., antibiotic resistance, in the plastisphere. However, the impact of plastic-antibiotic tandem on the soil ecosystem functioning, particularly on microbial function and metabolism remains currently unexplored. Herein, we investigated the competence of soil bacteria to colonize plastics and degrade 13C-labeled sulfamethoxazole (SMX). Using single-cell imaging, isotope tracers, soil respiration and SMX mineralization bulk measurements we show that microbial colonization of polyethylene (PE) and polystyrene (PS) surfaces takes place within the first 30 days of incubation. Morphologically diverse microorganisms were colonizing both plastic types, with a slight preference for PE substrate. CARD-FISH bacterial cell counts on PE and PS surfaces formed under SMX amendment ranged from 5.36 × 103 to 2.06 × 104, and 2.06 × 103 to 3.43 × 103 hybridized cells mm−2, respectively. Nano-scale Secondary Ion Mass Spectrometry measurements show that 13C enrichment was highest at 130 days with values up to 1.29 atom%, similar to those of the 13CO2 pool (up to 1.26 atom%, or 22.55 ‰). Independent Mann-Whitney U test showed a significant difference between the control plastisphere samples incubated without SMX and those in 13C-SMX incubations (P < 0.001). Our results provide direct evidence demonstrating, at single-cell level, the capacity of bacterial colonizers of plastics to assimilate 13C-SMX from contaminated soils. These findings expand our knowledge on the role of soil-seeded plastisphere microbiota in the ecological functioning of soils impacted by anthropogenic stressors.",

keywords = "Antibiotics, Biofilm formation, FISH-SIP-nanoSIMS, Plastics, Single-cell imaging, Sulfamethoxazole degradation",

author = "Qian Xiang and Hryhoriy Stryhanyuk and Matthias Schmidt and Steffen K{\"u}mmel and Richnow, {Hans H.} and Zhu, {Yong Guan} and Li Cui and Niculina Musat",

note = "Publisher Copyright: {\textcopyright} 2024 Elsevier Ltd",

year = "2024",

month = aug,

doi = "10.1016/j.envpol.2024.124197",

language = "English",

volume = "355",

journal = "Environmental Pollution",

issn = "0269-7491",

publisher = "Elsevier Ltd",

}

Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole. / Xiang, Qian; Stryhanyuk, Hryhoriy; Schmidt, Matthias et al.
In: Environmental Pollution, Vol. 355, 124197, 08.2024.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole

AU - Xiang, Qian

AU - Stryhanyuk, Hryhoriy

AU - Schmidt, Matthias

AU - Kümmel, Steffen

AU - Richnow, Hans H.

AU - Zhu, Yong Guan

AU - Cui, Li

AU - Musat, Niculina

PY - 2024/8

Y1 - 2024/8

N2 - The presence and accumulation of both, plastics and antibiotics in soils may lead to the colonization, selection, and propagation of soil bacteria with certain metabolic traits, e.g., antibiotic resistance, in the plastisphere. However, the impact of plastic-antibiotic tandem on the soil ecosystem functioning, particularly on microbial function and metabolism remains currently unexplored. Herein, we investigated the competence of soil bacteria to colonize plastics and degrade 13C-labeled sulfamethoxazole (SMX). Using single-cell imaging, isotope tracers, soil respiration and SMX mineralization bulk measurements we show that microbial colonization of polyethylene (PE) and polystyrene (PS) surfaces takes place within the first 30 days of incubation. Morphologically diverse microorganisms were colonizing both plastic types, with a slight preference for PE substrate. CARD-FISH bacterial cell counts on PE and PS surfaces formed under SMX amendment ranged from 5.36 × 103 to 2.06 × 104, and 2.06 × 103 to 3.43 × 103 hybridized cells mm−2, respectively. Nano-scale Secondary Ion Mass Spectrometry measurements show that 13C enrichment was highest at 130 days with values up to 1.29 atom%, similar to those of the 13CO2 pool (up to 1.26 atom%, or 22.55 ‰). Independent Mann-Whitney U test showed a significant difference between the control plastisphere samples incubated without SMX and those in 13C-SMX incubations (P < 0.001). Our results provide direct evidence demonstrating, at single-cell level, the capacity of bacterial colonizers of plastics to assimilate 13C-SMX from contaminated soils. These findings expand our knowledge on the role of soil-seeded plastisphere microbiota in the ecological functioning of soils impacted by anthropogenic stressors.

AB - The presence and accumulation of both, plastics and antibiotics in soils may lead to the colonization, selection, and propagation of soil bacteria with certain metabolic traits, e.g., antibiotic resistance, in the plastisphere. However, the impact of plastic-antibiotic tandem on the soil ecosystem functioning, particularly on microbial function and metabolism remains currently unexplored. Herein, we investigated the competence of soil bacteria to colonize plastics and degrade 13C-labeled sulfamethoxazole (SMX). Using single-cell imaging, isotope tracers, soil respiration and SMX mineralization bulk measurements we show that microbial colonization of polyethylene (PE) and polystyrene (PS) surfaces takes place within the first 30 days of incubation. Morphologically diverse microorganisms were colonizing both plastic types, with a slight preference for PE substrate. CARD-FISH bacterial cell counts on PE and PS surfaces formed under SMX amendment ranged from 5.36 × 103 to 2.06 × 104, and 2.06 × 103 to 3.43 × 103 hybridized cells mm−2, respectively. Nano-scale Secondary Ion Mass Spectrometry measurements show that 13C enrichment was highest at 130 days with values up to 1.29 atom%, similar to those of the 13CO2 pool (up to 1.26 atom%, or 22.55 ‰). Independent Mann-Whitney U test showed a significant difference between the control plastisphere samples incubated without SMX and those in 13C-SMX incubations (P < 0.001). Our results provide direct evidence demonstrating, at single-cell level, the capacity of bacterial colonizers of plastics to assimilate 13C-SMX from contaminated soils. These findings expand our knowledge on the role of soil-seeded plastisphere microbiota in the ecological functioning of soils impacted by anthropogenic stressors.

KW - Antibiotics

KW - Biofilm formation

KW - FISH-SIP-nanoSIMS

KW - Plastics

KW - Single-cell imaging

KW - Sulfamethoxazole degradation

UR - http://www.scopus.com/inward/record.url?scp=85193960897&partnerID=8YFLogxK

U2 - 10.1016/j.envpol.2024.124197

DO - 10.1016/j.envpol.2024.124197

M3 - Journal article

C2 - 38782163

AN - SCOPUS:85193960897

SN - 0269-7491

VL - 355

JO - Environmental Pollution

JF - Environmental Pollution

M1 - 124197

ER -

Stable isotopes and nanoSIMS single-cell imaging reveals soil plastisphere colonizers able to assimilate sulfamethoxazole

Abstract

Keywords

Access to Document

Other files and links

Fingerprint

Cite this