The surface roughness of bacteria affects the attachment of marine nanoparticles to bacteria
―Contribution to a detailed understanding of bacterial nutrient acquisition strategies and biogeochemical cycles in the ocean―

1. Key Points

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Previously, little was known about the cell surface roughness of marine bacteria (*1) or how it affects the attachment of nanoparticles, an important nutrient resource for bacteria

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The surface roughness of bacteria collected from the coastal and pelagic ocean regions of Japan and California (USA) was measured at the nanoscale using an atomic force microscope (*2), and the distribution and variation were determined

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Incubation experiments with bacterial isolates and model nanoparticles revealed that bacterial surface roughness has a significant impact on nanoparticle attachment to bacteria

2. Overview

Using atomic force microscopy, Yosuke Yamada, a researcher at the Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), the Japan Agency for Marine-Earth Science and Technology (JAMSTEC), and his colleagues discovered that the surface roughness of marine bacteria varies greatly from cell to cell, with a difference of more than 10 times in the root mean square roughness. Furthermore, incubation experiments with bacterial isolates and model nanoparticles revealed that surface roughness affects nanoparticle attachment to bacterial cells. These findings will not only deepen our understanding of the bacterial strategies for nutrient acquisition but also help clarify the mechanism of material cycles in the ocean.

The aforementioned study was published in Limnology and Oceanography by the Association for the Sciences of Limnology and Oceanography on January 27, 2023 (JST). This study was supported by JSPS KAKENHI (grant numbers JP19H05667, JP20K19960, and JP21H03586), JST FOREST (grant number JPMJFR2070), and the Gordon and Betty Moore Foundation Marine Microbial Initiative (grant number 4827).

3. Background

Over the past 3.8 billion years, bacteria have evolved their cell surfaces to utilize food particles efficiently. As there are approximately one million bacteria per mL of seawater, they have the largest reactive surface in the ocean and utilize about half of the carbon fixed by phytoplankton photosynthesis. Organic nanoparticles primarily derived from phytoplankton and bacteria (e.g., cell debris, polysaccharides, nucleic acids, proteins, etc.) are abundant in seawater and are considered important nutrient resources for bacteria. However, the mechanism by which bacteria utilize nanoparticles in seawater is poorly understood.

The first step in the bacterial utilization of nanoparticles is the attachment of nanoparticles to the bacterial surface, which is affected by various factors such as the structure, composition, and charge of the bacterial membrane surface, as well as the amount of exopolymer on bacterial cells. From a physical perspective, nanoscale roughness, one of the bacterial surface properties, increases or decreases the surface area of bacteria and can alter the repulsive interaction energy barrier between nanoparticles and attachment surfaces. These properties suggest that bacterial surface roughness is a dynamic parameter that reflects species, growth stage, and environmental conditions and may regulate the attachment of nanoparticles to bacteria.

4. Results

The bacterial surface roughness of over 1,000 cells collected from the coastal and pelagic ocean regions of Japan and California (USA) was measured using atomic force microscopy and found to be highly variable between cells (Fig. 1a–c). In addition, there was a negative relationship between roughness and water temperature (Fig. 1d). It is still a hypothesis, but this relationship may be a reflection of the viscosity of seawater and the collision frequency of nanoparticles and bacterial cells. This is because when the water temperature is low, the seawater becomes more viscous and the collision frequency decreases, whereas when the water temperature increases, the viscosity decreases, and the collision frequency increases (the Stokes–Einstein model). To survive in these environments, marine bacteria may alter the surface roughness and adjust the acquisition efficiency of nanoparticles.

Incubation experiments with bacterial isolates (Vibrio sp. and Alteromonas sp.) revealed that the surface roughness of bacteria also varies depending on the growth phase and species, with few exceptions (Fig. 2). Furthermore, incubation experiments with marine viral assemblages and polystyrene beads as model nanoparticles revealed a positive correlation between the bacterial surface roughness and the number of nanoparticles attached to bacteria, indicating that the rougher the cell surface, the more nanoparticles attached (Fig. 3). These findings indicate that bacterial surface roughness is one of the parameters regulating nanoparticle attachment to bacterial cells.

As described above, bacterial surface roughness is a dynamic parameter that varies according to environmental factors such as water temperature as well as bacterial growth phases and species. It largely affects the acquisition of nanoparticles, an important nutrient resource for bacteria. These findings are expected to contribute to the understanding of bacterial nutrient acquisition strategies and marine biogeochemical cycles in the ocean.

5. Future perspectives

In this study, we measured the surface roughness of marine bacterial assemblages and isolates collected from the surface of the ocean and investigated its role in nanoparticle attachment. However, the effect of water temperature and the surface properties of bacteria in the deep ocean on nanoparticle attachment is still unknown. It is also unclear whether the relationship between roughness and nanoparticle attachment can be applied to other bacterial species. Elucidating these unanswered questions are anticipated to lead to a deeper comprehension of how bacterial surface properties affect bacterial survival strategies and marine material circulation.

Fig.1　Comparison of the surface roughness and various environmental factors of natural bacterial assemblages collected from coastal and pelagic ocean areas shallower than 10 m. It shows that the surface roughness of cells is highly variable and tends to decrease with increasing water temperature.

Fig.2　Surface roughness of bacterial isolates (Vibrio sp., SWAT3; Alteromonas sp., TW7 and AltSIO) at various growth phases (E, S). It shows that bacterial surface roughness varies based on bacterial species and growth phases.

Fig.3　Relationship between bacterial surface roughness and attachment of nanoparticles to cells. Natural virus assemblages and polystyrene beads were used as model nanoparticles and were cultured with bacterial isolates (SWAT3 and TW7). Surface roughness and nanoparticle attachment to bacterial cells (scavenging) showed a positive linear relationship for both bacterial species and model nanoparticles, suggesting that bacterial surface roughness is a parameter regulating nanoparticle attachment.