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. 2021 Jul 15;10(28):e00498-21. doi: 10.1128/MRA.00498-21

Coding-Complete Genome Sequences of 11 SARS-CoV-2 B.1.1.7 and B.1.351 Variants from Metro Manila, Philippines

John Mark Velasco a,c,✉, Piyawan Chinnawirotpisan a, Maria Theresa Valderama a, Khajohn Joonlasak a, Wudtichai Manasatienkij a, Angkana Huang a, Paula Corazon Diones a, Fatima Claire Navarro b, Vicente Vila II b, Henry Tabinas Jr b, Domingo Chua Jr b, Stefan Fernandez a, Anthony Jones a, Chonticha Klungthong a
Editor: Simon Rouxd
PMCID: PMC8281087  PMID: 34264104

ABSTRACT

Here, we report the complete genome sequences of 11 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants from the Philippines. Lineage analysis showed 3 B.1.1.7 and 8 B.1.351 sequences. One B.1.1.7 sequence contained two additional mutations, F318N and V320F, with V320F located in the receptor binding domain of the S1 subunit.

ANNOUNCEMENT

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), belonging to the family Coronaviridae and the genus Betacoronavirus, is the causative agent of coronavirus disease 2019 (COVID-19) in humans (1). The first case of the SARS-CoV-2 B.1.1.7 variant was detected in a Filipino returning from the United Arab Emirates who arrived in the Philippines on 7 January 2021 (2, 3). The B.1.351 and the P.1. variants were detected by early March (4, 5) from returning overseas Filipino workers (3–5). Here, we announce the genome sequences of 11 SARS-CoV-2 strains collected from 12 March to 8 April 2021 from COVID-19 reverse transcription-PCR (RT-PCR)-positive Filipino patients (4). Viral RNA was extracted from nasopharyngeal/oropharyngeal swabs using a QIAamp viral RNA minikit (Qiagen) and used as the template for amplicon sequencing using ARTIC SARS-CoV-2 v3 primers (6). DNA libraries were constructed and multiplexed using the Illumina DNA preparation kit and then pooled before sequencing. Sequencing was performed on the iSeq100 platform using the iSeq reagent kit v2 (Illumina, USA) at the AFP-AFRIMS Molecular Laboratory, V. Luna Medical Center, Quezon City, Philippines. Primer region trimming and variant calling (Phred quality [Q] score, ≥25) were performed using iVAR v1.2.2 (7) and SAMtools (8), respectively. Consensus sequences were generated using iVAR v1.2.2 (7) (Q, ≥25; depth of coverage, ≥10×). Gaps, deletions, and ambiguous bases were identified and confirmed by genome-guided assembly using the reference sequence (GenBank accession no. NC_045512.2) with Trinity v2.11.0 (9). The lineage and clade were determined using Pangolin v2.1.10 (10) and GISAID clade nomenclature (11). MAFFT v7.475 (12) was used to examine the nucleotide and amino acid substitutions. All tools were run with default parameters. The raw reads yielded a total of 1.03 gigabases (84.3% of the clusters with Q ≥ 30). The lengths of the reads obtained were 35 to 151 nucleotides, and the range of the number of reads obtained per library was 2.4 million to 11.1 million reads. The consensus sequence lengths were similar to those of strain Wuhan-Hu-1 (NC_045512.2), with the mean coverage ranging from 563× to 2,469×. Table 1 shows the strain details and mutations. In total, 3/11 genomes were classified under clade GRY/lineage B.1.1.7, and 8/11 genomes were classified under clade GH/lineage B.1.351. All of the 11 sequenced samples collected from 12 March to 8 April 2021 were either B.1.1.7 or B.1.351 variants and were collected from patients with no history of travel, which suggests sustained, increasing community transmission and high numbers of these variants in the National Capital Region (NCR) starting in early March 2021. Both the B.1.351 and B.1.1.7 variants have been associated with increased transmissibility (13, 14), reduced neutralizing titers, reduced vaccine efficacy (15–21), and significantly higher adjusted odds ratio for hospitalization and intensive care admission (22). We compared the S gene mutations in our sequences with 542,800 B.1.1.7 and 14,359 B.1.351 GISAID sequences accessed on 8 May 2021 using outbreak.info (23), and one of our B.1.1.7 sequences (MZ068158) contained two unique mutations, F318N and V320F. The F318N mutation was located in an unknown function region between the N-terminal domain and the receptor binding domain, while the V320F mutation was located in the receptor binding domain in the S1 subunit. The surge of COVID-19 cases starting in early March 2021 (24) in the NCR may be explained by the circulation of these variants in addition to the relaxation of quarantine measures, increased mobility of the population, and lower compliance with health standards. Informed consent was obtained from the patients for SARS-CoV-2 real-time RT-PCR (rRT-PCR) testing and sequencing. The sample collection was considered a public health effort and did not require an institutional review board-approved human use protocol.

TABLE 1.

Genome features of 11 SARS-CoV-2 samples from the National Capital Region, Philippines

Sequence name GenBank accession no. SRA accession no. Collection date (day-mo-yr) Patient data
 Ct valueb Genome size (bp) GC content (%) Mean depth of coverage (×) Coveragec (%) Clade Lineage Gene region Nucleotide substitutiond Amino acid substitutiond
Sexa Age (yr) Location Symptoms Clinical outcome
SARS-CoV-2/Philippines/AFRIMS-COVID51005 MZ068151 SRR14460628 12-Mar-21 M 55 Quezon City, National Capital Region None No data 21.72 29,885 39 1,648 99.5 GH B.1.351 ORF1a 1059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
SARS-CoV-2/Philippines/AFRIMS-COVID52511 MZ068152 SRR14460627 18-Mar-21 M 46 Pasay City, National Capital Region Fever, cough, sore throat, diarrhea, body malaise, anosmia Quarantine, discharged stable 19.25 29,885 38 1,618 99.7 GH B.1.351 ORF1a 1059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
N 28928: C > A L219I
ORF14 28928: C > A L65L
SARS-CoV-2/Philippines/AFRIMS-COVID53359 MZ068153 SRR14460625 20-Mar-21 F 51 Taguig City, National Capital Region Fever, chills, runny nose, cough Admitted to hospital, discharged stable 23.29 29,885 39 563 95.3 GH B.1.351 ORF1a 1 059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5144: C > T L1627L
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
SARS-CoV-2/Philippines/AFRIMS-COVID53656 MZ068154 SRR14460624 22-Mar-21 M 56 Taguig City, National Capital Region Difficulty breathing Diagnosed with pulmonary tuberculosis and pneumonia; admitted to hospital and discharged stable 22.01 29,885 39 2,468 98.9 GH B.1.3 51 ORF1a 1059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17577: A > G E1370E
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23277: C > T T572I
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28093: C > T S67F
ORF8 28253: C > T F120F
N 28887: C > T T205I
ORF14 28887: C > T L52F
SARS-CoV-2/Philippines/AFRIMS-COVID53909 MZ068155 SRR14460623 22-Mar-21 M 24 Taguig City, National Capital Region Fever, cough, general weakness, sore throat, vomiting Home quarantine, stable, recovered 25.95 29,884 39 1,768 96.7 GRY B.1.1.7 ORF1a 913: C > T S216S
ORF1a 3037: C > T F924F
ORF1a 3267: C > T T1001I
ORF1a 5388: C > A A1708D
ORF1a 5986: C > T F1907F
ORF1a 6954: T > C I2230T
ORF1a 7097: A > G I2278V
ORF1a 11114: G > A G3617S
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 14676: C > T P403P
ORF1b 15279: C > T H604H
ORF1b 16176: T > C T903T
ORF1b 17615: A > G K1383R
ORF1b 19079: A > G E1871G
ORF1b 19854: C > T D2129D
S Deletion 21765–21770 HV position 69–70
S Deletion 21991–21993 Y position 144
S 23063: A > T N501Y
S 23271: C > A A570D
S 23403: A > G D614G
S 23604: C > A P681H
S 23709: C > T T716I
S 24506: T > G S982A
S 24914: G > C D1118H
ORF8 27972: C > T Q27*
ORF8 28048: G > T R52I
ORF8 28111: A > G Y73C
Nontranslation region Deletion 28271 NAe
N 28280: G > C NA
N 28281: A > T D3L
N 28282: T > A NA
N 28881: G > A R203K
N 28882: G > A NA
N 28883: G > C G204R
ORF14 28881: G > A NA
ORF14 28882: G > A G50N
ORF14 28883: G > C NA
N 28977: C > T S235F
SARS-CoV-2/Philippines/AFRIMS-COVID55604 MZ068156 SRR14460622 26-Mar-21 M 28 Tanay, Rizal, Calabarzon (Region 4-A) None Home quarantine, stable, recovered 19.66 29,885 39 1,254 96.6 GH B.1.351 ORF1a 1059: C > T T265I
ORF1a 1441: C > T G392G
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
SARS-CoV-2/Philippines/AFRIMS-COVID56628 MZ068157 SRR14460621 29-Mar-21 M 44 Tanay, Rizal, Calabarzon (Region 4-A) Cough, fever, anosmia, diarrhea Diagnosed with pneumonia, admitted to hospital, discharged stable 20.50 29,885 39 2,261 96.2 GH B.1.351 ORF1a 1059: C > T T265I
ORF1a 2195: G > A D644N
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 9559: C > T Y3098Y
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1a 12008: C > T L3915F
ORF1a 12641: C > A L4126I
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF6 27213: C > T L4L
ORF8 28253: C > T F120F
ORF8 28254: A > C I121L
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
SARS-CoV-2/Philippines/AFRIMS-COVID58228 MZ068158 SRR14460620 7-Apr-21 M 43 Navotas City, National Capital Region Colds, cough, anosmia, diarrhea Home quarantine, stable, recovered 28.31 29,884 39 2,158 97.3 GRY B.1.1.7 ORF1a 816: G > A R184H
ORF1a 913: C > T S216S
ORF1a 3037: C > T F924F
ORF1a 3267: C > T T1001I
ORF1a 5388: C > A A1708D
ORF1a 5986: C > T F1907F
ORF1a 6954: T > C I2230T
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 14676: C > T P403P
ORF1b 15096: T > C N543N
ORF1b 15279: C > T H604H
ORF1b 16176: T > C T903T
ORF1b 16323: C > T C952C
S Deletion 21765–21770 HV position 69–70
S Deletion 21991–21993 Y position 144
S 22514: T > A F318N
S 22515: T > A F318N
S 22520: G > T V320F
S 23063: A > T N501Y
S 23271: C > A A570D
S 23403: A > G D614G
S 23604: C > A P681H
S 23709: C > T T716I
S 24109: C > T L849L
S 24506: T > G S982A
S 24914: G > C D1118H
ORF3a 25427: C > T T12I
ORF7a 27503: C > T S37F
ORF8 27972: C > T Q27c
ORF8 28048: G > T R52I
ORF8 28095: A > T K68c
ORF8 28111: A > G Y73C
Nontranslation region Deletion 28271 NA
N 28280: G > C NA
N 28281: A > T D3L
N 28282: T > A NA
N 28881: G > A R203K
N 28882: G > A NA
N 28883: G > C G204R
ORF14 28881: G > A NA
ORF14 28882: G > A G50N
ORF14 28883: G > C NA
N 28977: C > T S235F
SARS-CoV-2/Philippines/AFRIMS-COVID58236 MZ068159 SRR14460619 7-Apr-21 M 39 Paco, Manila City, National Capital Region Cough Home quarantine, stable, recovered 24.47 29,884 39 1,695 97.6 GRY B.1.1.7 ORF1a 816: G > A R184H
ORF1a 913: C > T S216S
ORF1a 3037: C > T F924F
ORF1a 3267: C > T T1001I
ORF1a 5388: C > A A1708D
ORF1a 5986: C > T F1907F
ORF1a 6954: T > C I2230T
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 14676: C > T P403P
ORF1b 15096: T > C N543N
ORF1b 15279: C > T H604H
ORF1b 16176: T > C T903T
ORF1b 16323: C > T C952C
S Deletion 21765–21770 HV position 69–70
S Deletion 21991–21993 Y position 144
S 23063: A > T N501Y
S 23271: C > A A570D
S 23403: A > G D614G
S 23604: C > A P681H
S 23709: C > T T716I
S 24109: C > T L849L
S 24506: T > G S982A
S 24914: G > C D1118H
ORF3a 25427: C > T T12I
ORF7a 27503: C > T S37F
ORF8 27972: C > T Q27*
ORF8 28048: G > T R52I
ORF8 28095: A > T K68*
ORF8 28111: A > G Y73C
Nontranslation region Deletion 28271 NA
N 28280: G > C NA
N 28281: A > T D3L
N 28282: T > A NA
N 28881: G > A R203K
N 28882: G > A NA
N 28883: G > C G204R
ORF14 28881: G > A NA
ORF14 28882: G > A G50N
ORF14 28883: G > C NA
N 28977: C > T S235F
SARS-CoV-2/Philippines/AFRIMS-COVID58693 MZ068160 SRR14460618 8-Apr-21 F 47 Caloocan City, National Capital Region Fever Home quarantine, stable, recovered 17.92 29,885 38 1,939 98.9 GH B.1.351 ORF1a 337: C > G R24R
ORF1a 1059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
SARS-CoV-2/Philippines/AFRIMS-COVID58620 MZ068161 SRR14460626 8-Apr-21 F 26 Indang, Cavite, Calabarzon (Region 4-A) None No data 23.26 29,903 39 1,961 98.5 GH B.1.351 ORF1a 1059: C > T T265I
ORF1a 3037: C > T F924F
ORF1a 4213: T > C A1316A
ORF1a 5230: G > T K1655N
ORF1a 10323: A > G K3353R
ORF1a 11812: C > A G3849G
ORF1a 12159: A > G E3965G
ORF1b Deletion 11288–11296 SGF position 3675–3677
ORF1b 14408: C > T P314L
ORF1b 15925: C > T L820F
ORF1b 17970: T > C D1501D
S 21641: G > T A27S
S 21801: A > C D80A
S 22206: A > G D215G
S Deletion 22281–22289 LLA position 241–243
S 22813: G > T K417N
S 23012: G > A E484K
S 23063: A > T N501Y
S 23403: A > G D614G
S 23664: C > T A701V
S 23764: A > T T734T
ORF3a 25546: C > T L52F
ORF3a 25563: G > T Q57H
ORF3a 25904: C > T S171L
E 26456: C > T P71L
ORF8 28253: C > T F120F
N 28642: T > C Y123Y
N 28887: C > T T205I
ORF14 28887: C > T L52F
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a

M, male; F, female.

b

Ct, threshold cycle.

c

The strain Wuhan-Hu-1 (GenBank accession no. NC_045512.2) reference genome was used for estimation of the horizontal coverage.

d

Unique mutations are in bold.

e

NA, not applicable.

Data availability.

The SARS-CoV-2 genome sequences from the Philippines were deposited in the GenBank database (accession no. MZ068151 to MZ068161). The raw reads have been deposited in the NCBI Sequence Read Archive (SRA accession no. SRR14460618 to SRR14460628). The BioProject accession number is PRJNA726840. The BioSample accession numbers are SAMN18976036 to SAMN18976046.

ACKNOWLEDGMENTS

We acknowledge the Department of Research and Training, the Department of Pathology and Laboratory Medicine, and the Hospital Infection Control Committee of the V. Luna Medical Center (Quezon City, Philippines) for support with the specimen collection. The material has been reviewed by the Walter Reed Army Institute of Research. There is no objection to its presentation and/or publication. The opinions or assertions contained herein are our private views and are not to be construed as official or as reflecting the true views of the Department of the Army or the Department of Defense. The investigators have adhered to the policies for the protection of human subjects as prescribed in AR 70–25.

This study was funded by the Armed Forces Health Surveillance Division and its Global Emerging Infections Surveillance Branch, USA, under grant no. P0103_21_AF (COVID-19 Supplemental: AFRIMS Virology Regional COVID-19 Surveillance and Characterization Program) and P0084_21_AF (Respiratory Work Plan) for fiscal year (FY) 2021. We declare no competing interests.

Contributor Information

John Mark Velasco, Email: velascojm@afrims.org.

Simon Roux, DOE Joint Genome Institute.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The SARS-CoV-2 genome sequences from the Philippines were deposited in the GenBank database (accession no. MZ068151 to MZ068161). The raw reads have been deposited in the NCBI Sequence Read Archive (SRA accession no. SRR14460618 to SRR14460628). The BioProject accession number is PRJNA726840. The BioSample accession numbers are SAMN18976036 to SAMN18976046.

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