Bacterial Communities of Ixodes scapularis from Central Pennsylvania, USA
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sample Collections
2.2. DNA Extraction
2.3. Sample Preparation for Sequencing
2.4. Analysis of Microbiome Sequence Data
2.5. Taxon-Specific Amplification and Sequence Confirmation
2.6. Assays for Tick-Borne Pathogens
2.6.1. Borrelia burgdorferi Infection Frequency
2.6.2. Taqman PCR Assay for Anaplasma phagocytophilum
2.7. Taxon-Specific Quantitative PCR of Nonpathogenic Symbiotic Bacteria
3. Results
3.1. Sequencing of Individual and Pooled Tick DNA Using V6 Hypervariable Region
3.2. Bacterial Community Composition of Pooled Tick DNA Using the V4 Hypervariable Region
3.3. Sex- and Location-Specific Differences in Microbial Diversity
3.4. Confirmation by Gene-Specific Amplification and Sequencing
3.5. Confirmation of Borrelia burgdorferi Identification and Frequency in Ticks Tested
3.6. Taxon-Specific Quantitative PCR
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Collection Year | Sample ID | Population | Sex | Individuals or Pools Sequenced (N) | Region Sequenced (V4 or V6) |
---|---|---|---|---|---|
2012 | BHF01-F10 | Big Hollow (BH) | Females | Individuals (10) | V6 |
2012 | BHM01-M10 | Big Hollow (BH) | Males | Individuals (10) | V6 |
2012 | SCF01-F10 | Shaver’s Creek (ShCr) ª | Females | Individuals (10) | V6 |
2013 | MB001 | Stormstown (Sto) | Females | Pooled (20) | V4/V6 |
2013 | MB002 | Stormstown (Sto) | Males | Pooled (20) | V4/V6 |
2013 | MB004 | Blue Course (BC) | Females | Pooled (18) | V4/V6 |
2013 | MB003 | Blue Course (BC) | Males | Pooled (15) | V4/V6 |
2013 | MB006 | AgProgressDays (APD) | Females | Pooled (16) | V4/V6 |
2013 | MB005 | AgProgressDays (APD) | Males | Pooled (14) | V4/V6 |
2013 | MB008 | Big Hollow (BH) | Females | Pooled (20) | V4/V6 |
2013 | MB007 | Big Hollow (BH) | Males | Pooled (15) | V4/V6 |
2013 | MB009 | Galbraith (Gal) | Females | Pooled (20) | V4/V6 |
2013 | MB010 | Galbraith (Gal) | Males | Pooled (20) | V4/V6 |
2013 | MB012 | Benner Springs (Ben) | Females | Pooled (20) | V4/V6 |
2013 | MB011 | Benner Springs (Ben | Males | Pooled (20) | V4/V6 |
2013 | MB013 | State Gameland 176 (SGL176/Sco) | Females | Pooled (20) | V4/V6 |
2013 | MB014 | State Gameland 176 (SGL176/Sco) | Males | Pooled (20) | V4/V6 |
2014 | MB015 | Shaver’s Creek (ShCr) | Females | Pooled (20) | V4/V6 |
2014 | MB016 | Shaver’s Creek (ShCr) | Males | Pooled (20) | V4/V6 |
2014 | Lem | Lemont b | Females | Pooled (3F) | V4/V6 |
2014 | PGM | Pine Grove Mills b | Mixed | Pooled (4F, 4M) | V4/V6 |
2014 | Toft | Toftrees b | Mixed | Pooled (11F, 9M) | V4/V6 |
2009 | MS1 | Mississippi clade 1 (F3, F5, G4, G6) c | Females | Pooled (4) | V4/V6 |
2009 | MS2 | Mississippi clade 2 (F6, F8, G11) d | Females | Pooled (3) | V4/V6 |
Taxon | Primer Name | Target Gene | Size (bp) | Primer Sequence (5′ → 3′) | Reference |
---|---|---|---|---|---|
Anaplasma phagocytophilum | ApMSP2f | Msp2 (major surface protein 2) | 77 | ATGGAAGGTAGTGTTGGTTATGGTATT | [23] |
ApMSP2r | TTGGTCTTGAAGCGCTCGTA | ||||
Ap Taqman probe | ApMSP2p | /HEX/TGGTGCCAG/ZEN/GGTTGAGCTTGAGATTG/IABkFQ | |||
Borrelia burgdorferi | PC-1s | OspC | 632 | AATGAAAAAGAATACATTAAGTGCA | [24] |
PC-2a | OspC | TTAAGGTTTTTTTGGACTTTCTGC | |||
Borrelia burgdorferi | BBSCH31 | FlaB (outer) | 437 | CACACCAGCATCACTTTCAGGGTCT | [25] |
BBSCH42 | FlaB (outer) | CAACCTCATCTGTCATTGTAGCATCTTTTATTT | |||
Borrelia burgdorferi | FL59 | FlaB (inner) | 277 | GCATTTTCAATTTTAGCAAGTGATG | [25] |
FL7 | FlaB (inner) | TTTCAGGGTCTCAGGCGTCTT | |||
Candidatus Cardinium | CLOf | 16S rRNA | 1100 | GCGGTGTAAAATGAGCGTG | [26] |
CLOr2 | 16S rRNA | ACCTMTTCTTAACTCAAGCCT | |||
Chalcidoideae | 1775-COIF | COI | 1047 | CGA- ATAAATAATATAAGATTTTG | [27] |
2773-COI-R | COI | GGATAATCTCTATATCGACGAGGTAT | |||
Flavobacterium | qFlav16SF | 16S rRNA | 142 | CGATGGATACTAGCTGTTGGG | This study |
qFlav16SR | 16S rRNA | CGAATTAAACCACATGCTCCAC | |||
Ixodes scapularis | IsActin2F | Actin | 271 | GACCTGACCGACTACCTGATGAAG | This study |
IsActin2R | Actin | ATGCCGCACGATTCCATACC | |||
Ixodiphagus hookeri | 401-F | COI | 268 | TTTAGAATATTTATTGATTCAGGGACT | [28] |
44-R | CTCCTGCTAAAACTGGTAAAGATAAT | ||||
Legionellales | RLrpoB6f | rpoB | 729 | AGATGGTACGCSGGTTGATATCGT | [29] |
RLrpoB2r | rpoB | TTCCATTTGGTGATCGCCATC | |||
Nematode | Nema12SF | 12S | 450 | GTT CCA GAA TAA TCG GCT A | [30] |
Nema12SR | ATT GAC GGA TG(AG) TTT GTA CC | ||||
Pseudomonas | PA-GS-F | 16S rRNA | 618 | GACGGGTGAGTAATGCCTA | [31] |
PA-GS-R | 16S rRNA | CACTGGTGTTCCTTCCTATA | |||
Pseudomonas | 16S qPCR_F | 16S rRNA | 143 | TTGTCCTTAGTTACCAGCACG | This study |
16S qPCR_R | 16S rRNA | ACCCTTTGTACCGACCATTG | |||
Rickettsia | r190.7 | RompA | 632 | ATGGCGAATATTTCTCCAAAA | [32] |
r190.701 | RompA | GTTCCGTTAATGGCAGCATCT | |||
Rrgap2F | RompA | 1664 | CTACCTTGTACCTTGCTGAGCGAAA | This study | |
Rrgap2R | AGCTTTGCAGCTAACGGCGCT | ||||
Rickettsia | qRi16SF | 16S rRNA | 124 | ACCTTACCAACCCTTGACATG | This study |
qRi16SR | GGACTTAACCCAACATCTCACG | ||||
Rickettsiella | qRkla6F | 16S rRNA | 135 | AAAGGAATTGACGGGGGCC | This study |
qRkla6F | CCTGTCTCTTGGTTCCTTTCGG | ||||
Wolbachia | wsp 81F | wsp | 610 | TGG TCC AAT AAG TGA TGA AGA AAC | [33] |
wsp 691R | wsp | AAA AAT TAA ACG CTA CTC CA |
qPCR | PCR | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Population | Sex | I/P (N) | Ap MSP2 | qRi | qRk5 | qRk6 | qPs | qFl | FlaB | OspC | RompA | RLrpo | CLO | Nema | Chal |
Stormstown | Female | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Stormstown | Males | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
BlueCourse | Males | P (15) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
BlueCourse | Female | P (18) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
APDS | Males | P (14) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
APDS | Female | P (16) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Big Hollow | Males | P/I (15) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
I (20) | ☑ | ☑ | |||||||||||||
Big Hollow | Female | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Galbraith | Female | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Galbraith | Males | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
I (20) | ☑ | ☑ | |||||||||||||
Benner Springs | Males | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Benner Springs | Female | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
SGL176 | Female | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
SGL176 | Males | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Shaver’s Creek | Female | P/I (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
I (20) | ☑ | ☑ | |||||||||||||
Shaver’s Creek | Males | P (20) | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ | ☑ |
Julian, PA 2015 | Females | P (16) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Julian, PA 2015 | Males | P (20) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
SGL333_2017 | Females | P (20) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
SGL333_2017 | Males | P (20) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
SGL333_2018 | Females | P (50) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
SGL333_2018 | Males | P (40) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Howard, PA | Females | P (9) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Howard, PA | Males | P (15) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Lederer Park, State College | Females | P (21) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Lederer Park, State College | Males | P (21) | ☑ | ☑ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ | ☐ |
Taxon | Gene | Genbank Accession Number |
---|---|---|
Rickettsia | RompA | JFKF01000169.1, LN794217.1, CP003340.1, CP047359.1, CP003375.1, CP040325.1, CP001612.1, CP003308.1, CP001227.1, CP012420.1, CP000683.1, CP003342.1 |
Rickettsiella | rpoB | KP985349.1, KP985348.1, KP985347.1, KP985346.1, KP985354.1, KP985353.1, EF694042.1, JF288929.1, KP985351.1, KP985350.1, AP018005.1, KP985357.1, KP985356.1, KP985355.1 |
Cardinium | 16S rRNA | AB241135.1, AB241129.1, GU731426.1, AB241131.1, AB241130.1, AY753169.1, MH057615.1, AY635291.1, AB001518.1, LN829689.2, JN204482.1, LC159289.1, AB241132.1, AF350221.1, AB116514.1, KX022134.1, AB506775.1, AB506773.1, AB506774.1, GQ206320.1, CP022339.1 |
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Sakamoto, J.M.; Silva Diaz, G.E.; Wagner, E.A. Bacterial Communities of Ixodes scapularis from Central Pennsylvania, USA. Insects 2020, 11, 718. https://doi.org/10.3390/insects11100718
Sakamoto JM, Silva Diaz GE, Wagner EA. Bacterial Communities of Ixodes scapularis from Central Pennsylvania, USA. Insects. 2020; 11(10):718. https://doi.org/10.3390/insects11100718
Chicago/Turabian StyleSakamoto, Joyce Megumi, Gabriel Enrique Silva Diaz, and Elizabeth Anne Wagner. 2020. "Bacterial Communities of Ixodes scapularis from Central Pennsylvania, USA" Insects 11, no. 10: 718. https://doi.org/10.3390/insects11100718
APA StyleSakamoto, J. M., Silva Diaz, G. E., & Wagner, E. A. (2020). Bacterial Communities of Ixodes scapularis from Central Pennsylvania, USA. Insects, 11(10), 718. https://doi.org/10.3390/insects11100718