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Brief Report

Population Dynamics and Feeding Preferences of Three Bacterial-Feeding Nematodes on Different Bacteria Species

by
Yiqun Zhou
1,2,
Hao Zheng
1,2,
Dandan Gao
1,2,3,* and
Jie Zhao
2,4,5,6,*
1
Faculty of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004, China
2
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China
3
National Engineering Laboratory for Applied Technology of Forestry & Ecology in South China, Central South University of Forestry and Technology, Changsha 410004, China
4
Guangxi Industrial Technology Research Institute for Karst Rocky Desertification Control, Nanning 530012, China
5
Guangxi Key Laboratory of Karst Ecological Processes and Services, Huanjiang 547100, China
6
Huanjiang Observation and Research Station for Karst Ecosystems, Chinese Academy of Sciences, Huanjiang 547100, China
*
Authors to whom correspondence should be addressed.
Agronomy 2023, 13(7), 1808; https://doi.org/10.3390/agronomy13071808
Submission received: 5 June 2023 / Revised: 27 June 2023 / Accepted: 6 July 2023 / Published: 7 July 2023
(This article belongs to the Section Pest and Disease Management)
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Abstract

:
Soil food webs are extremely complex as they contain diverse organisms. Feeding preference, also known as prey selection, is an important determinant of soil community compositions. However, the feeding preferences of nematodes are commonly ignored in ecology research. In this paper, the population dynamics and feeding preferences of three bacterial-feeding nematodes (i.e., Caenorhabditis elegans, Protorhabditis spp., and Acrobeloides spp.) for eight bacterial prey species were evaluated. Protorhabditis and Acrobeloides were isolated from a paddy soil in subtropical China. C. elegans, the most common model system for biological research, was used as a control in this study, and it was revealed that C. elegans could feed on all the eight bacteria strains. Protorhabditis could only survive when fed E. coli and Bacillus thuringiensis. Acrobeloides could only survive when fed E. coli and B. aryabhattai. During 10 days of culture, C. elegans populations reached the maximum in 5–7 days, and most C. elegans populations exceeded 10,000 individuals. The two Protorhabditis populations on E. coli and Bacillus thuringiensis included less than 800 individuals during 10 days of culture. Acrobeloides population on B. aryabhattai reached the maximum (7799 individuals) on day 8, while on E. coli was its population included less than 500 individuals. These results indicate that different nematode species indeed have distinct feeding preferences. In addition, the population dynamics of the two soil nematodes isolated from soil could not fully match with their inferred life-history strategies (i.e., cp values, and a 1-5 colonizer-p-ersister series that range from r-strategists to K-strategists). Our findings highlights the existing deficiencies in the understanding of the feeding behavior and the life-history strategies of soil nematodes.

1. Introduction

Nematodes in the soil are highly diverse, particularly the bacterivorous nematodes [1,2,3]. They play a vital role in regulating soil bacterial communities, as well as, soil nutrient cycling [4]. Different bacterivorous nematode taxa have different influences on bacterial communities. For example, there are taxa that exploit enriched media rapidly and have high fertility rates and other taxa that feed continuously as resource changes but have relatively low fertility rates. Different species of nematodes exhibit a wide range of life-history strategies, including colonizer-persister (cp) ranging from 1 (typical r strategy) to 5 (typical K strategy) [5,6]. The r strategies prioritize rapid reproduction in unstable environments, while the K strategies emphasize quality offspring and resource competition in stable environments [7]. The cp values are widely used in soil nematode community analysis by calculating a series of maturity indices [8,9,10]. The cp values are generally inferred and are constant for the same nematode genus [9,11]. However, this assumption overlooks the diverse feeding preferences of nematodes and the complex interactions that occur between nematodes and other soil organisms, which can vary depending on the composition of the microbial community [12]. Particularly, the cp values of many soil nematode genera do not correspond to their responses to resource enrichment or disturbance [13,14]. Therefore, it is necessary to improve the knowledge of the population dynamics and feeding preferences of nematodes.
Understanding of soil nematode population dynamics and feeding preferences is significant for nematode ecology, particularly in studies of soil food web trophic interactions and the use of nematodes as ecological indicators. Soil bacterial-feeding nematodes feed on a wide range of bacteria, and the nematodes will select those that are favorable for growth and reproduction in preference to others [15,16,17]. Selective feeding by Caenorhabditis elegans (Maupas, 1900) Daugherty, 1959, significantly affects its metabolism, the level of mitochondrial DNA replication, and its longevity and egg production [18]. The bacterial-feeding nematodes prefer to feed on Gram-negative (G−) bacteria rather than Gram-positive (G+) bacteria, which may be due to thinner cell wall and potential ease of digestion of the G− bacteria [16,19]. Due to its short life cycle and ease of cultivation, C. elegans has become a model organism used in many laboratories around the world [20]. However, little is known about the population dynamics and feeding preferences of other soil dwelling nematodes feeding on different bacteria as well as the differences in population dynamics between nematodes feeding on the same species of bacteria.
In this study, we conducted a series of Petri dish experiments to explore the population dynamics and feeding preferences of two bacterivorous nematode species (i.e., Protorhabditis spp. and Acrobeloides spp.) extracted from paddy soils in subtropical China. As a control, the population dynamics and feeding preferences of C. elegans were also monitored. According to the nematode colonizer–persister theory, cp1 type nematodes are characterized by short generation times and explosive population growth in conditions of food abundance. On the other hand, cp2 type nematodes also have short generation times and relatively high reproduction rates, but these rates are not as high as those observed in cp1-type nematodes [21]. In addition, the cp2 nematodes are very tolerant to adverse conditions and feed more deliberately and continue feeding even as resources decline [6]. Protorhabditis spp. and C. elegans are cp1 type and Acrobeloides spp. is the cp2 type [11,21]. In this study, eight species of bacteria were used as prey, seven of which were isolated from the paddy soil. We hypothesized that (1) the Protorhabditis spp. (cp1) population developed more rapidly than the Acrobeloides spp. (cp2) population and that (2) the feeding preferences of the three nematodes may be different and G− bacteria will be preferred over G+ bacteria.

2. Materials and Methods

2.1. Preparation of Nematodes

Three nematode species, C. elegans (wild type), Acrobeloides spp., and Protorhabditis spp., were tested in the present study. The C. elegans used in this study was purchased from a C. genetics center (CGC) user on a Chinese online retailer (Taobao, China). The Acrobeloides spp. and Protorhabditis spp. were extracted from a paddy soil collected on 8 October 2022 from a rice (Oryza sativa L.)-sorghum (Sorghum bicolor L.) Moench rotation field of the Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha city, Hunan Province, China. The paddy soil is classified as Ultisol [22]. The modified Baermann funnel method was used to extract the nematodes for 48 h. The turbid nematode suspensions were cleaned using the method of low-temperature settling and centrifugation [23]. Then, the nematodes were further cleaned to remove surface microorganism using sterile water for 30 s to 60 s. Selected nematodes were then transferred to a prepared nematode growth medium (NGM) (Shanghai Ruichubio Biotech Co., Ltd., Shanghai, China) that had been inoculated with E. coli op50 and cultured at a constant temperature of 25 °C [24]. With a stereomicroscope, individuals with the same morphological traits were chosen for transfer to the new NGM until the entire NGM was populated with a single taxon of worms. After being studied under an inverted microscope, the morphological characteristics were eventually recognized as belonging to Acrobeloides spp. and Protorhabditis spp.

2.2. Preparation of the Bacteria

In this study, a total of eight bacteria were used as nematode prey, seven of which were isolated from the same soil as the nematodes, while the other one was Escherichia coli OP50 obtained from the Key Laboratory of Agro-ecological Processes in Subtropical Region (Table 1). The steps for isolating bacteria from soil were as follows: the soil was cultured in a LB medium after leaching dilution, and then monoclonal colonies were picked in a new LB medium. After incubation, sixteen monoclonal colonies with sufficient biomass were obtained, which were identified and analyzed by Beijing Tsingke Biotech Co., Ltd., Beijing, China. DNA was extracted from strain samples, amplified and sequenced using common primers for bacterial 16S, and the sequencing results were used for comparison in the NCBI database to the samples that were initially identified using the NCBI database. Seven bacterial species were identified in the sixteen colonies, which were Bacillus. sp. A1-S8, Bacillus cereus AP12, Bacillus aryabhattai ZJJH-2, Bacillus thuringiensis AK08, Lysinibacillus macroides DST15, Dyella sp. BAB-4442, and Burkholderia sp. Ellin155.

2.3. Nematode Population Dynamic Experiment: Experiment 1

At total of 120 NGM Petri dishes were used in this study. There were 5 replicates for each combination of 3 nematode species and 8 bacteria species. Particularly, each of the cultured bacteria strains was inoculated on 15 NGM Petri dishes, which were used for culturing the three species of nematodes. The NGM Petri dishes inoculated with bacteria were kept in a 37 °C incubator. After 48 h culturing, each Petri dish received 30 nematodes of the same species (C. elegans, Acrobeloides spp. or Protorhabditis spp.). One nematode at a time was aspirated with a pipette and deposited in the Petri dish. Then, the nematode Petri dishes were incubated at 25 °C for ten days and the number of nematodes in each Petri dish was recorded daily with a stereomicroscope (M165FC, Leica Microsystems (Switzerland) Ltd., Heerbrugg, Switzerland).

2.4. Feeding Preference Experiment of C. elegans: Experiment 2

A total of 8 NGM Petri dishes were used in this experiment. Each dish was evenly divided into 8 zones (Supporting information, Figure S1). Suspension of each of the eight bacteria (10 μL) were pipetted into the center of the 8 designated zones in each Petri dish. The NGM Petri dishes were kept in a 37 °C incubator and cultured for 48 h. Each Petri dish was subsequently inoculated with a population of 100 C. elegans nematodes via pipette, which were placed on the center of the Petri dish (Supporting information, Figure S1). Then, the Petri dishes were incubated at 25 °C for 24 h. The number of nematodes that migrated to each designated bacterial zone was recorded at 2, 4, 8, 12, and 24 h with a stereomicroscope (M165FC, Leica Microsystems (Switzerland) Ltd., Heerbrugg, Switzerland). In this study, only C. elegans was used for feeding preference experiments. The Protorhabditis spp. and Acrobeloides spp. could only survive on two bacteria species of which only one was isolated from the paddy soil in experiment 1 in this study. Using the eight bacteria species to test the feeding preferences of the Protorhabditis and Acrobeloides was not practical. Given the fact that these two nematodes can only survive on one bacteria species isolated from paddy soil, any observations addressing the feeding preferences of the Protorhabditis and Acrobeloides on the other soil bacteria in the paddy soils may lead to wrong conclusions.

2.5. Statistical Analysis

Repeated measure ANOVAs were used to investigate the nematode population dynamics by examining the time effect and treatment effect (i.e., different bacterial prey) on the three nematode species through the 10-day period of culturing experiment (experiment 1). Repeated measure ANOVAs were also used to examine the feeding preference of C. elegans by comparing the numbers of nematodes in different bacterial colony zones during the 24 h period of culturing experiment (experiment 2). One-way ANOVAs were used to compare the differences in the C. elegans numbers in eight bacterial colony zones at each monitoring time in experiment 2. Before analysis, data were natural log or square root-transformed when required to improve normality and homogeneity of variance. Differences among treatments was determined via the least significant difference (LSD) multi-comparison test. Statistical significance was determined at p < 0.05. All statistical analyses were performed using SPSS 27.0 (IBM SPSS Inc., Chicago, IL, USA).

3. Results

In experiment 1, C. elegans survived and fed on all the eight bacterial species and all displayed unimodal patterns during the 10-day culture period (Figure 1a). Caenorhabditis elegans on E. coli reached maximum population size with 13,639 individuals at day 5. The C. elegans on Dyella sp., Burkholderia sp., Bacillus sp., L. macrolides, B. aryabhattai, and B. thuringiensis reached maximum population size at day 7 with 20,804, 15,451, 14,531, 12,524, 12,976, and 15,587, respectively (Figure 1a). The C. elegans on B. cereus reached maximum population size at day 7–9 with 7505–7869 individuals. Repeated measure ANOVA showed that there were significant differences between C. elegans population on E. coli and those on Bacillus sp. and B. cereus (Figure 1a). There was also a significant difference of C. elegans population on Bacillus sp. from that on B. thuringiensis (Figure 1a). Additionally, there were significant differences of C. elegans population on B. cereus from those on Burkholderia sp., B. aryabhattai, and B. thuringiensis (Figure 1a). Protorhabitis could only survive on E. coli and B. thuringiensis and continuously increased to 638 and 697 individuals at the end of the culturing period, respectively (Figure 1b). Repeated measure ANOVA showed that the differences were not significant between the two populations of Protorhabitis (Figure 1b). Acrobeloides could only survive on E. coli and B. aryabhattai (Figure 1c). In addition, the population of Acrobeloides on B. aryabhattai displayed a unimodal pattern with a maximum size of 7799 individuals at day 8 (Figure 1c). The population of Acrobeloides on E. coli continuously increased to about 700 individuals at the end of the culture period (Figure 1c). Repeated measure ANOVA showed that there was a significant difference between the two populations of Acrobeloides (Figure 1b).
In the feeding preference experiment of C. elegans, one-way ANOVA results showed that the numbers of C. elegans were significantly higher in the colony zone of B. thuringiensis than those in the other bacterial colony zones in 2 h monitoring time (Figure 2). After that, the number of C. elegans progressively decreased to a very low level in the colony zone of B. thuringiensis (Figure 2). In 4 and 8 h monitoring times, the numbers of C. elegans in colony zone of Dylla sp. were apparently higher than those in the other bacterial colony zones; however, it was significantly decreased in 12 h monitoring time (Figure 2). The numbers of C. elegans in colony zones of E. coli, Burkholderia sp., and L. macroides were progressively increased during the 24 h monitoring (Figure 2). At the end of the experiment, the numbers of C. elegans in colony zones of E. coli, Dylla sp., Burkholderia sp., and L. macrolides were significantly higher than those in the other four bacterial colonies (Figure 2), and the number of C. elegans in colony zone of E. coli was significantly higher than those in the L. macrolides colony (Figure 2). Repeated measure ANOVAs showed that the numbers of C. elegans in colony zones of E. coli and Dylla sp. were significantly higher than those in the L. macrolides, Bacillus sp., B. cereus, B. aryabhattai, and B. thuringiensis colonies (Figure 2). In addition, the numbers of C. elegans in colony zones of Burkholderia sp. and L. macrolides were significantly higher than those in the Bacillus sp. and B. aryabhattai colonies (Figure 2).

4. Discussion

The population dynamics of nematodes are different when feeding on different species of bacteria. The finding is consistent with previous studies that reported different population dynamics among nematodes consuming different species of bacteria, including C. elegans, Protorhabditis spp., and Acrobeloides spp. [18,25]. Surprisingly, the Protorhabditis spp. and Acrobeloides spp. could only survive on one of the seven soil bacteria prey isolated from the paddy soil in this study. In addition, the Acrobeloides that fed on B. aryabhattai could reach maximum population size around 8000 individuals in day 8. However, Protorhabditis that fed on B. thuringiemsis only had fewer than 800 individuals during 10-day culturing and did not reach a maximum population size. These results indicate that different species of soil nematodes may prey on different bacteria species in soil. The trophic interactions between bacterivorous nematodes and bacteria may be species-specific. In other words, numerous statistical correlations between bacteria species and bacterivorous nematode species, as depicted in soil biota co-occurrence networks, may not actually reflect trophic interactions [26]. In addition, the finding was inconsistent with the hypothesis I that the Protorhabditis spp. (cp1) population developed more rapidly than the Acrobeloides spp. (cp2) population. One likely reason is that the most preferred bacterial prey species for Protorhabditis was not isolated from the paddy soil in this study. Another possible explanation is that the inferred cp values or life-history strategies of the Protorhabditis and Acrobeloides were not accurate. Many previous studies reported that the commonly used cp value assignments (or inferred life history strategies) of some nematode species were inconsistent with their responses to nutrient enrichment or ecological disturbances [13,14,27]. Therefore, the cp values for particular nematode taxa still need to be modified through time [9]. Moreover, the population dynamics of Protorhabditis and Acrobeloides were similar when they fed on E. coli that was not isolated from the paddy soil in this study (Supporting information, Figure S2). This results further confirmed that the inferred cp values for nematodes need to be modified, especially for the Protorhabditis in this study.
Although only eight bacteria species were tested as bacterivorous nematode prey, a pattern of nematode feeding preferences for G− bacteria was found, especially for C. elegans. Particularly, colony zones of G− bacteria had more nematodes than those of G+ bacteria in experiment 2. This finding is consistent with hypothesis II. Similar results were also obtained in the population dynamics experiment (experiment 1, just like this study where the maximum population sizes of C. elegans on G− bacteria were greater than that on G+ bacteria. Consistent with our findings, previous studies reported that soil bacterial-feeding organisms prefer G− bacteria over G+ bacteria [19,28]. This is most likely because the thinner cell walls of G− bacteria which make them more readily to be digested [16,29]. Unfortunately, the Protorhabditis spp. and Acrobeloides spp. could only survive on two bacterial preys of which only one was isolated from the paddy soil in this study. It was unsound to use the eight bacterial preys to test the feeding preferences of the Protorhabditis spp. and Acrobeloides spp. The use of only one soil bacteria species as prey for each nematode species is insufficient for a thorough examination of feeding preferences. Based on the population dynamic results, the population dynamics of Protorhabditis spp. had similar patterns on G+ (B. thuringiensis) and G− (E. coli) bacterial prey, and the population of Acrobeloides spp. grew more rapidly on the G+ bacteria (B. aryabhattai) than the G− bacteria (E. coli). Therefore, different nematodes may have different preferences for G− versus G+ bacteria in soil habitat. Our findings do not support the viewpoint that soil bacterivorous nematodes have feeding preferences on G− bacteria over G+ bacteria.
In summary, this study found that different species of nematodes exhibit species-specific trophic interactions with different species of bacteria, indicating that the statistical correlations (e.g., co-occurrence network analysis) between bacteria and nematode species may not reflect actual trophic interactions. This is because many statistical correlations may be indirect interactions (not feeding relationship), which is influenced by other factors, such as environmental conditions and the presence of other organisms. In addition, population dynamics of both the cp1 nematode (Protorhabditis) and the cp2 nematode (Acrobeloides) were inconsistent with their inferred life-history strategies. Therefore, the cp values for particular nematode taxa still need to be modified with time. Moreover, our study did not provide solid evidence on the feeding preferences of soil nematodes for G− bacteria. One limitation of this study is that the size of bacterial prey pool was small, with only eight species. Moreover, the Protorhabditis spp. and Acrobeloides spp. could only feed and survive only on two bacteria preys. Therefore, the present study highlights the need for additional research to improve our understanding of feeding behavior and life-history strategies of soil nematodes on more species of bacteria prey.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13071808/s1, Figure S1: Diagram of the Petri dish zoning for the C. elegans feeding preference experiment. Figure S2: The population dynamics of C. elegans, Protorhabditis spp., and Acrobeloides spp. feeding on E. coli. during 10-day culturing period. Error bars represent standard errors.

Author Contributions

Conceptualization, J.Z. and D.G.; methodology, J.Z.; software, Y.Z. and H.Z.; validation, Y.Z., H.Z., J.Z. and D.G.; formal analysis, Y.Z.; investigation, Y.Z. and H.Z.; resources, J.Z. and D.G.; data curation, Y.Z. and J.Z.; writing—original draft preparation, Y.Z.; writing—review and editing, J.Z. and D.G.; visualization, Y.Z. and J.Z.; supervision, D.G.; project administration, J.Z. and D.G.; funding acquisition, J.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Key R&D Program of China (2022YFD1901000); the National Natural Science Foundation of China (U21A20189); the Natural Science Foundation for Distinguished Young Scholars of Hunan Province (2021JJ10042); the Guangxi Key Research and Development Plan (AB20297004); the program of the Youth Innovation Promotion Association of Chinese Academy of Sciences (Y201969); and the Guangxi Bagui Scholarship Program given to Dejun Li.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, Jie Zhao, upon reasonable request.

Acknowledgments

We thank the Institutional Center for Shared Technologies and Facilities of Institute of Subtropical Agriculture, CAS Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for their help in soil sample analysis.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 13 01808 g001 550
Figure 1. The population dynamics of C. elegans (a), Protorhabditis spp. (b), and Acrobeloides spp. (c) feeding on eight bacterial prey species during 10-day culturing. Error bars represent standard errors.
Figure 1. The population dynamics of C. elegans (a), Protorhabditis spp. (b), and Acrobeloides spp. (c) feeding on eight bacterial prey species during 10-day culturing. Error bars represent standard errors.
Agronomy 13 01808 g001
Agronomy 13 01808 g002 550
Figure 2. The number of C. elegans recorded in the eight bacterial zones in 2, 4, 8, 12, and 24 h in the nematode feeding preference experiment (experiment 2). Error bars represent standard errors.
Figure 2. The number of C. elegans recorded in the eight bacterial zones in 2, 4, 8, 12, and 24 h in the nematode feeding preference experiment (experiment 2). Error bars represent standard errors.
Agronomy 13 01808 g002
Table
Table 1. Eight bacterial species used in this study.
Table 1. Eight bacterial species used in this study.
AbbreviateSpecies aPhylumShapeGram StainAccession Number b
E. cEscherichia coliProteobacteriarodG−-
D. sDyella sp.ProteobacteriarodG−MK825220
Bu. sBurkholderia sp.ProteobacteriarodG−AF408997
Ba. sBacillus sp.FirmicutesrodG+JX994094
L. mLysiniBacillus macroidesFirmicutesrodG+MN474024
B. cBacillus cereusFirmicutesrodG+MT598023
B. aBacillus aryabhattaiFirmicutesrodG+MT605509
B. tBacillus thuringiensisFirmicutesrodG+MT598028
a E. coli was obtained from the Key Laboratory of Agro-ecological Processes in Subtropical Region. The other seven species were isolated from a subtropical paddy soil in the Institute of Subtropical Agriculture, Chinese Academy of Sciences. The seven isolated bacteria were identified via 16S rRNA genes using the Sanger sequencing method by (Beijing Tsingke Biotech Co., Ltd., Beijing, China. b The GeneBank accession number of the 16S rRNA gene sequence.
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Zhou, Y.; Zheng, H.; Gao, D.; Zhao, J. Population Dynamics and Feeding Preferences of Three Bacterial-Feeding Nematodes on Different Bacteria Species. Agronomy 2023, 13, 1808. https://doi.org/10.3390/agronomy13071808

AMA Style

Zhou Y, Zheng H, Gao D, Zhao J. Population Dynamics and Feeding Preferences of Three Bacterial-Feeding Nematodes on Different Bacteria Species. Agronomy. 2023; 13(7):1808. https://doi.org/10.3390/agronomy13071808

Chicago/Turabian Style

Zhou, Yiqun, Hao Zheng, Dandan Gao, and Jie Zhao. 2023. "Population Dynamics and Feeding Preferences of Three Bacterial-Feeding Nematodes on Different Bacteria Species" Agronomy 13, no. 7: 1808. https://doi.org/10.3390/agronomy13071808

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