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5Russian Journal of Nematology, 2021, 29 (1), 23 - 29
Bacteria associated with plant tissues infected
by plant-parasitic nematodes from families Anguinidae Nicoll, 1935 and Aphelenchoididae
Skarbilovich, 1947
Irina P. Starodumova1, Lubov V. Dorofeeva1, Vladimir N. Chizhov2, Steven A. Nadler3, Sergei A. Subbotin2, 3' 4 and Lyudmila I. Evtushenko1
1All-Russian Collection of Microorganisms (VKM), G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Scientific Centre for Biological Research, Russian Academy of Sciences, Pushchino, Russia 2A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia 3Department of Entomology and Nematology, University of California, Davis, California, USA 4California Department of Food and Agriculture, Sacramento, California, USA e-mail: [email protected]
Accepted for publication 25 March 2021
Summary. A total of 38 bacterial strains were isolated from 23 samples of plants infected by 17 species of nematodes from the genera Anguina, Heteroanguina, Mesoanguina, Ditylenchus and Aphelenchoides. The 16S rRNA gene-based identification revealed that the strains belonged to 11 genera of the classes Alphaproteobacteria (Sphingomonas, Caulobacter, Rhizobium), Bacilli (Bacillus, Paenibacillus, Lactococcus, Staphylococcus) and Actinobacteria (Rathayibacter, Brachybacterium, Mycolicibacterium, Plantibacter). The isolated strains showed high 16S rRNA gene sequence identity (99.1-100%) to 19 type strains of validly described species, which indicates that they match known species or are closely related novel (not yet validly described) species. Among the species comprising the aforementioned bacterial genera, only several species of Rathayibacter and Sphingomonas are plant pathogens. Some of the known species of Staphylococcus and the other revealed genera that include human pathogens, were reported to show plant growth-promoting properties.
Key words: 16S rRNA gene, Actinobacteria, Alphaproteobacteria, Anguina, Aphelenchoides, Bacilli, Ditylenchus, Heteroanguina, Mesoanguina, plant pathogen.
It has been shown by several studies that parasitic nematodes inducing swellings and galls in plants are often associated with specific bacteria, and that such bacteria-nematode associations are widespread (Evtushenko et al., 1994; Evtushenko & Takeuchi, 2006). Some seed gall and foliar nematodes act as specific vectors of bacterial plant pathogens and an obligate aetiological relationship is established between the two, resulting in manifestation of a new disease syndrome in host plants (Taylor, 1990). Plant pathogenic species of the genus Rathayibacter and other genera of the family Microbacteriaceae (Actinobacteria) or putative new species of the same family with unproven pathogenicity are often found in plants infected by plant-parasitic nematodes of the genera Anguina, Mesoanguina and Aphelenchoides (Evtushenko & Takeuchi, 2006; Murray et al., 2017;
Starodumova et al., 2017; Tarlachkov et al., 2020). The goal of this study was to screen for presence of species of Rathayibacter and other bacterial genera in herbarium plant materials and in materials freshly collected in areas naturally infested by plant-parasitic nematodes of the genera Anguina, Heteroanguina, Mesoanguina, Ditylenchus and Aphelenchoides.
MATERIAL AND METHODS
Nematode sample collection. Plant nematode galls and other plant samples infected with nematodes were obtained from colleagues or collected from natural areas. Samples were kept in dry condition in paper envelopes. In total, twenty-three herbarium accessions were used for isolation of bacteria (Table 1).
© Russian Society of Nematologists, 2021; doi: 10.24411/0869-6918-2021-10003
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Table 1. Identification of bacteria isolated from plants infected by nematodes of the families Anguinidae and Aphelenchoididae on the basis of 16S rRNA gene sequences.
Sample number Nematode Host plant name Host plant family Plant organ Country Bacterium strain number GenBank accession number Closest type strain 16S rRNA gene sequence identity (%) and size (bp) Class
Family Anguinidae
34 Afrina sporoboliae Sporobolus cryptandrus Poaceae Seed gall USA, Idaho CA-741 MT853077 Rathayibacter agropyri CA-4T 99.1% (1418) Actinobacteria
39 Afrina wevelh Eragrostis curvula Poaceae Seed gall South Africa CA-833 MT853111 Sphingomonas leidyi ATCC 15260T ' 100% (1431) Alpliaproteobacteria
60 Anguilla agropyri Elytrigia repens Poaceae Stem gall Russia CA-764 MT853096 Sphingomonas zeae JM-7911 100% (1367) Alpliaproteobacteria
60 A. agropyri Elytrigia repens Poaceae Stem gall Russia CA-765 MT853097 Caulobacter vibrioides CB51T 99.49% (1407) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-762 MT853094 Sphingomonas zeae JM-7911 99.9% (1341) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-763 MT853095 Sphingomonas leidyi ATCC 15260T ' 100% (1442) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-775 MT853081 Sphingomonas leidyi ATCC 15260T ' 100% (618) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-776 MT853082 Sphingomonas zeae JM-7911 99.7% (1341) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-779 MT853090 Sphingomonas melonis DAPP-PG 224T 99.49% (1206) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-817 MT853078 Sphingomonas leidyi ATCC 15260T ' 100% (649) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-818 MT853080 Sphingomonas leidyi ATCC 15260T ' 100% (656) Alpliaproteobacteria
38 A. agrostis Agrostis sp. Poaceae Seed gall Brazil CA-840 MT853079 Sphingomonas leidyi ATCC 15260T ' 100% (1383) Alpliaproteobacteria
33 A. funesta Lolium rigidum Poaceae Seed gall Australia CA-778 MT853089 Staphylococcus pasteuri ATCC 51129T 99.9% (1437) Bacilli
31 Angllina sp. Astrebla pectinata Poaceae Seed gall Australia CA-766 MT853098 Sphingomonas zeae JM-7911 100% (1250) Alpliaproteobacteria
31 Angllina sp. A. pectinata Poaceae Seed gall Australia CA-774 MT853106 Rhizobium metallidurans ChimEc512T 99.9% (1408) Alpliaproteobacteria
58 Angllina sp. Dactyhs glomerata Poaceae Seed gall USA, Oregon CA-770 MT853102 Sphingomonas zeae JM-7911 100% (1367) Alpliaproteobacteria
58 Angltina sp. D. glomerata Poaceae Seed gall USA. Oregon CA-835 MT853112 Caulobacter vibrioides CB51T 99.5% (1439) Alpliaproteobacteria
63 Angllina sp. Acrocladium cuspidatum Amblyst egiaceae Leaf gall Estonia CA-771 MT853103 Bacillus subtilis subsp. subtilis NCIB 3610T 99.9% (1420) Bacilli
Table 1 (continued). Identification of bacteria isolated from plants infected by nematodes of the families Anguinidae and Aphelenchoididae on the basis of 16S rRNA gene sequences.
57 Heteroanguina graminophila Calamagrostis sp. Poaceae Leaf gall Russia, Moscow CA-768 MT853100 Bacillus megaterium NBRC 15308T 100% (1408) Bacilli
57 H. graminophila Calamagrostis sp. Poaceae Leaf gall Russia, Moscow CA-769 MT853101 Staphylococcus warneri ATCC 27836T 100% (1447) Bacilli
43 H. graminophila Calamagrostis sp. Poaceae Leaf gall Russia, Far East CA-828 MT853110 Mycolicibacterium aurum NCTC 10437T 100% (1475) Actinobacteria
32 Mesoanguina chilensis Nothofagus pumilia Nothofagaceae Leaf gall Chile CA-791 MT853085 Lactococcus lactis subsp. lactis JCM 5805T 100% (1434) Bacilli
37 M. mobilis Arctotheca calendula Asteraceae Leaf gall Australia CA-780 MT853088 Sphingomonas zeae JM-7911 100% (1367) Alphaproteobacteria
61 M. moxae Artemisia rubripes Asteraceae Leaf gall Russia CA-767 MT853099 Caulobacter vibrioides CB51T 99.5% (1439) Alphaproteobacteria
35 M. picridis Cousinia onopordioides Asteraceae Leaf gall Turkmenistan CA-788 MT853083 Sphingomonas leidyi ATCC 15260T ' 100% (511) Alphaproteobacteria
35 M. picridis C. onopordioides Asteraceae Leaf gall Turkmenistan CA-789 MT853084 Sphingomonas leidyi ATCC 15260T ' 100% (1442) Alphaproteobacteria
35 M. picridis C. onopordioides Asteraceae Leaf gall Turkmenistan CA-841 MT853091 Caulobacter vibrioides CB51T 99.5% (1316) Alphaproteobacteria
53 M. picridis Serratilla latifolia Asteraceae Leaf gall Iran CA-837 MT853114 Plantibacter flavus VKM Ac-2504T 100% (1420) Actinobacteria
14 Ditylenchus Rigas Vicia faba Fabaceae Stem gall Germany CA-772 MT853104 Bacillus aryabhattai B8W22T 100% (1438) Bacilli
14 D. gigas V. faba Fabaceae Stem gall Germany CA-773 MT853105 Bacillus megaterium NBRC 15308T 100% (1440) Bacilli
13 D. dipsaci V. faba Fabaceae Seed UK CA-758 MT853093 Paenibacillus tundrae A10bT 99.5% (1487) Bacilli
12 D. dipsaci Phlox sp. Polemoniaceae Stem gall Canada CA-792 MT853086 Bacillus megaterium NBRC 15308T 100% (1423) Bacilli
12 D. dipsaci Phlox sp. Polemoniaceae Stem gall Canada CA-793 MT853087 Bacillus megaterium NBRC 15308T 100% (868) Bacilli
Family Aphelenchoididae
20 Aphelenchoides fragariae Boykinia aconitifolia Saxifragaceae Leaf Germany CA-825 MT853108 Bacillus megaterium NBRC 15308T 100% (1450) Bacilli
23 A. ritzemobosi Doronicum Orientale Asteraceae Leaf Germany CA-781 MT853092 Staphylococcus epidermidis "NCTC 11047T 100% (1491) Bacilli
16 Aphelenchoides sp. Fem No data Leaf USA CA-839 MT853107 Bracliybacterium rhamnosum LMG 198481 99.8% (1474) Actinobacteria
71 Aphelenchoides sp. Tellima grandiflora Saxifragaceae Leaf USA CA-827 MT853109 Staphylococcus argenteus 'MSHR1132T 99.9% (1378) Bacilli
42 Aphelenchoides sp. Tanacetum sp. Asteraceae Leaf Russia CA-836 MT853113 Rathayibacter rathayi VKM Ac-1601T ' 99.8% (1299) Actinobacteria
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Isolation of bacteria. The air-dried plant samples infected by nematodes were soaked in sterile distilled water for 1 h, macerated, and washed twice in sterile distilled water. The washed samples were placed in 1 ml of 0.85% NaCl solution and milled. One drop (50 pl) of the obtained suspension was plated on R2A medium (Fluka Analytical, USA) and incubated for up to 3 weeks at room temperature (18-24°C). Bacteria from representative colonies were isolated after 1, 2 and 3 weeks and cultured on R2A medium.
DNA extraction. DNA was extracted from pure bacterial cultures grown on R2A agar for 2-3 days. One colony was put into 100 ^l ddH2O using a loop, vortexed, and incubated at 95°C for 15 min. After incubation, the tubes kept at -20°C until use.
PCR amplification, sequencing and molecular identification. For the 16S rRNA gene sequence study, 2 ^l of extracted DNA was transferred into a 0.2 ml Eppendorf tube containing 2.5 ^l 10* PCR buffer, 5 ^l Q solution (Qiagen), 0.5 ^l of dNTPs mixture (Taq PCR Core Kit, Qiagen), 0.15 ^l of each primer (1.0 ^g ^l-1), 0.1 ^l Taq polymerase, and 12.6 ^l distilled water. The PCR amplification profile consisted of 4 min at 94°C, 35 cycles of 1 min at 94°C, 1 min 30 s at 55°C, and 2 min at 72°C, followed by a final step of 10 min at 72°C. The 16S rRNA gene was amplified with the universal eubacterial 27F (5'-AGA GTT TGA TCC TGG CTC AG-3') and 1525R (5'-AAG GAG GTG ATC CAG CC-3') primers and sequenced using universal 785F (5'-GGM TTA GAT ACC TGG TAG TCC-3') and 907R (5'-CCG TCA ATT CCT TTG AGT TT-3') primers (Weisburg et al., 1991). PCR products were purified using QIAquick PCR Purification Kit (Qiagen) and directly sequenced. Sequencing was performed by Quintara Biosciences (CA, USA). The closest relatives and pairwise similarity of the 16S rRNA gene sequences was determined using EzBioCloud (Yoon et al., 2017). All new sequences obtained in this study were deposited in the GenBank database (Table 1).
RESULTS AND DISCUSSION
A total of 38 bacterial strains were isolated from 23 samples of plants infected by 17 nematode species belonging to the families Anguinidae and Aphelenchoididae (Table 1). The 16S rRNA gene-based identification using the EzBioCloud database (Yoon et al., 2017) revealed that the strains belonged to 11 genera of the classes Alphaproteobacteria (20 strains), Bacilli (13 strains), and Actinobacteria (5 strains). Most of the isolates were affiliated with the genus Sphingomonas (15 strains), followed by Bacillus (7 strains), Staphylococcus (4 strains),
Caulobacter (4 strains) and Rathayibacter (2 strains). Six genera were represented by a single isolate: Brachybacterium, Mycolicibacterium, Plantibacter, Rhizobium, Paenibacillus and Lactococcus. Members of the aforementioned 11 genera showed highest 16S rRNA gene sequence identity (99.1100%) to 19 type strains of validly described species (Table 1), which indicates that they match known species or are closely related novel (not yet validly described) species.
Strains of the genus Sphingomonas (Alphaproteobacteria) were most frequently isolated from galls induced by Anguina spp. and Afrina sp. on plants of the family Poaceae (Agrostis sp., Astrebla pectinata, Elytrigia repens, Eragrostis curvula, Dactylis glomerata) and from galls of Mesoanguina spp. on Asteraceae (Arctotheca calendula, Artemisia rubripes and Cousinia onopordioides). Four Caulobacter strains, also belonging to Alphaproteobacteria were found exclusively in plants of Poaceae and Asteraceae infested by Anguina spp. and Mesoanguina spp. By contrast, the endospore-forming bacteria of the genera Bacillus and Paenibacillus (Bacilli) tended to be associated mostly with plants infested by nematodes of the genera Ditylenchus and Aphelenchoides (6 out of 8 strains isolated) (Table 1).
These bacterial genera and many species comprising these genera are mostly known as biotechnologically and agriculturally important taxa (Sphingomonas spp., Bacillus spp., Paenibacillus spp.) or documented as human pathogens (Staphylococcus spp.) or commensals (Lactococcus spp., Staphylococcus spp.) (Yabuuchi & Kosako, 2015; Pérez-García et al., 2011; Grady et al., 2016; Olishevska et al., 2019). Several species of Rathayibacter and Sphingomonas are known as plant pathogens (Buonaurio et al., 2002; Evtushenko & Dorofeeva, 2012; Deldavleh et al., 2013; Kini et al., 2017; Murray et al., 2020). Some Caulobacter strains were reported to inhibit plant growth (Berrios & Ely, 2020).
Members of the aforementioned genera, including Staphylococcus, were also reported within plant tissues without causing any evident damage to the host, and showed plant growth-promoting properties. They play crucial roles in plant growth, development, fitness and protection using different mechanisms. Different plant growth-promoting properties of such endophytic bacteria have been described in many studies (Ulrich et al., 2008; Evtushenko & Dorofeeva, 2012; Phukon et al., 2013; De Meyer et al., 2015; Zhao et al., 2015; de Lacerda et al., 2016; Midha et al., 2016; Thomas & Sekhar, 2017; Gao et al., 2018; Marag & Suman, 2018; Tuo et al., 2018;
Berrios & Ely, 2020). Plant endophytic bacteria ubiquitously colonise a variety of internal plant tissues (intracellular or intercellular spaces) and are found in nearly every plant worldwide (Hallmann et al., 1997; Santoyo et al., 2016). Most species to which our isolates can be assigned (or are closely related to) occur, along with their usual habitat, in tissues of various plants, and some exhibited direct or indirect plant growth promoting properties as exemplified by Bacillus megaterium, B. subtilis, Lactococcus lactis, Plantibacter flavus, Staphylococcus epidermidis, S. pasteuri, Caulobacter vibrioides, and some others (Innerebner et al., 2011; Wang et al., 2013; de Lacerda et al., 2016; Zhao et al., 2015; Alibrandi et al., 2018; Marag & Suman, 2018; Gupta et al., 2019, Mayer et al., 2019; Ullah et al., 2019).
Three isolated strains showed closest 16S rRNA gene sequence identity to the plant pathogens in the genera Rathayibacter and Sphingomonas (Buonaurio et al., 2002; Evtushenko & Dorofeeva, 2012). These include Rathayibacter sp. CA-836 (99.8% identity to Rathayibacter rathayi), Rathayibacter sp. CA-741 (99.1% identity to Rathayibacter agropyri), and Sphingomonas sp. CA-779 (99.5% identity to Sphingomonas melonis). Rathayibacter rathayi is known to be nematode-associated and transmitted to host plants (wheat) by a seed gall nematode of the genus Anguina (Evtushenko & Dorofeeva, 2012). No precise data are available on the association of the two other plant pathogenic species, Rathayibacter agropyri (Murray et al., 2020) and Sphingomonas melonis (Buonaurio et al., 2002) with nematodes.
It is also worth noting that the bacteria identified here were recovered from plant samples that were stored at room temperatures for a long time, up to 67 years (seed galls on Elytrigia repens). The bacteria being in a hypobiotic state in dry plant samples are probably protected by the surrounding masses of dead bacterial and plant cells and some chemicals produced by bacteria and plants that assist bacteria to withstand drought stress (Lata et al., 2018; Ullah et al., 2019).
Further study of these and other bacteria from the nematode-infested plant tissues, including whole-genome sequencing, will reveal the nematode-associated bacterial diversity in plant microbiomes and specific bacterial-nematode plant pathogenic complexes. Such research also has the potential to provide insight into molecular mechanisms involved in interactions of bacteria, nematodes and plants.
ACKNOWLEDGEMENTS
This work was sponsored by the United States Department of Agriculture, Animal and Plant Health Inspection Service according to the research project AP18PPQS & T00C159 (18-0422-000-FR) "Enhancing diagnostics of plant pathogenic bacteria of the genus Rathayibacter'". The authors thank Drs T.D. Murray, I. Riley, M. Mundo-Ocampo, N. Vovlas and other colleagues for providing nematode infected plant materials.
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I.P. Starodumova, L.V. Dorofeeva, V.N. Chizhov, S.A. Nadler, S.A. Subbotin and L.I. Evtushenko.
Бактерии, ассоциированные с тканями растений, инфицированых фитопаразитическими нематодами из семейств Anguinidae Nicoll, 1935 и Aphelenchoididae Skarbilovich, 1947. Резюме. Из 23 изученных образцов растений, инфицированных нематодами 17 видов из родов Anguina, Heteroanguina, Mesoanguina, Ditylenchus и Aphelenchoides, было выделено 38 штаммов бактерий. Идентификация на основе гена 16S рРНК показала, что эти штаммы принадлежали к 11 родам классов Alphaproteobacteria (Sphingomonas, Caulobacter, Rhizobium), Bacilli (Bacillus, Paenibacillus, Lactococcus, Staphylococcus) и Actinobacteria (Rathayibacter, Brachybacterium, Mycolicibacterium, Plantibacter). Выделенные штаммы показали высокий уровень сходства с 19-ю типовыми штаммами валидно описанных видов по последовательностям генов 16S рРНК (99.1100%). Эти данные указывают на то, что изученные штаммы являются предствителями известных или еще не описанных новых видов. Среди видов, составляющих вышеупомянутые роды, только несколько видов Rathayibacter и Sphingomonas известны как патогены растений. Некоторые виды из выявленных родов, содержащих патогенов человека, включая род Staphylococcus, обладают свойствами, способствующими росту растений.
