PROBIOTIC GENOMES: SEQUENCING AND ANNOTATION IN THE PAST DECADE

PROBIOTIC GENOMES: SEQUENCING AND ANNOTATION IN THE PAST DECADE

Joel P. Joseph

Department of Genetic Engineering, SRM University, Kattankulathur - 603203, Tamil Nadu, India.

ABSTRACT: Probiotics are live microorganisms that confer many health benefits to the host when administered in adequate quantities. These health benefits have garnered much attention towards Probiotics and have given an impetus to their use as dietary supplements for the improvement of general health and as adjuvant therapies for certain diseases. The increased demand for probiotic products in the recent times has provided the thrust for probiotic research applied to several areas of human biology. The advances in genomic technologies have further facilitated the sequencing of the genomes of such probiotic bacteria and their genomic analyses to identify the genes that endow the beneficial effects they are known to exert. This work reviews the application of genomic strategies on probiotic bacteria, while providing the details about the probiotic strains whose genome sequences are available. It also consolidates the Genomic tools used for the sequencing, assembly and annotation of the probiotic genes and how it has helped in comparative genomic analyses.

Probiotics, Genome, Bacteria, Disease

INTRODUCTION: Probiotics can be defined as live non-pathogenic microorganisms that present health benefits to the host when administered in adequate quantities ^{1, 2}. They fall under the class of functional foods ^{3, 4}, and their health benefits encompass multiple facets of human health including improvement of intestinal health through the regulation of gut microflora ^{4 - 6}, prevention of enteric, respiratory tract, and urogenital infections ^{2, 4, 7, 8}, stimulation of immune system ⁹, anti-allergic activity ², anti-cancer effects ^{4, 7}, anti-microbial effects ^{10 - 12}, and cholesterol-lowering effects ^{13 - 16}. The growth of the global probiotic market has in turn served as an impetus to probiotic research driving the adoption of modern scientific technologies in studying the genetics and biology of probiotic microorganisms ³.

The term Probiotic finds its origin from the Greek words pro meaning for and biotikos meaning pertaining to life ¹⁷. With the earliest clues about the involvement of probiotics in health benefits dating back to the biblical times and the times of the ancient civilizations like the Roman empire, the history of probiotics go way back in time ¹⁸. The identification and isolation of gut microflora eventually paved way to the isolation of probiotic species and the study of their health benefits ^{4, 5, 17, 19, 20}. Among the bacterial species that fall under the spectrum of probiotics are the non-pathogenic species within the genera of Lactobacillus, Bifidobacterium, Clostridium, Bacillus, Escherichia, and Enterococcus ¹⁷. However, since several years, species within the genera of Lactobacillus and Bifidobacterium have dominated probiotic market²¹.

In the late 1990s and the early 2000, advances in sequencing technologies facilitated whole genome sequencing of several bacterial pathogens including Mycobaterium tuberculosis, Pseudomons aeroginosa, and enterohaemorrhagic Escherichia coli ^{22 - 24}.

In the recent past, however, the demand for probiotics has served as an impetus for the application of sequencing strategies and genomic technologies to obtain and analyze the whole genome sequences of several probiotic bacteria ^25-27. Thus, advances in genomic technologies and computational strategies have facilitated the characterization of microbial population, particularly probiotic bacteria ²⁸. The forthcoming section of this review articulates predominant probiotic species whose whole genome or draft genome sequences have been made available in public databases.

Genomic Technologies in Probiotic Research: One of the earliest whole genome sequencing projects of a probiotic species (Lactobacillus johnsonii NCC 533) was published as early as 2004 ²⁷. The sequencing strategy that was used for this project was the whole genome shotgun sequencing technology ²⁷. There on, several sequencing projects of probiotic genomes were published in the years that followed, with a rise in the number of such projects in the very recent years ^{25, 29 - 32}. Furthermore, there has been a gradual change in the sequencing technologies adopted overtime for such projects thus facilitating more genomes to be sequenced, assembled and annotated in shorter durations of time ^{25, 29 - 32}.

While initial genome sequencing strategies embraced the traditional Sanger sequencing methods ²⁵, more advanced sequencing technologies that are collectively referred to as the Next Generation Sequencing (NGS) technologies have been eventually adopted ^{26, 33- 35}. The genome sequencing of probiotic species until or before 2010 was accomplished by the traditional Sanger sequencing method and shotgun sequencing technique. These include the genome sequencing of Lactobacillus johnsonii NCC 533 and Bifidobacterium animalis subsp. lactis AD011^{25, 27}. Post 2010, NGS technologies have been adopted for genome sequencing with the prominent ones being 454 pyrosequencing technology, Illumina/ Solexa paired end sequencing technology, Ion Torrent sequencing technology, and Pacific BioSciences sequencing technology ^{26, 33-35}.

In 2011, most of the probiotic genomes were sequenced using Roche 454 GS FLX pyrosequencer. These include the genome sequences of Lactobacillus amylovorus ^{33, 36}, Lactobacillus ruminis³⁷, Lactobacillus coryniformis ³⁸, Lactobacillus animalis ³⁹, Lactobacillus cypricasei ⁴⁰, Lactobacillus sanfranciscensis ⁴¹, and Lactobacillus kefiranofaciens ³¹ among others. In some cases, a combination of two different sequencing technologies has been adopted. For instance, in case of Lactobacillus sanfranciscensis genome sequencing, a combination of Roche 454 GS FLX pyrosequencing technology and Sanger sequencing was adopted ⁴¹. Similarly, in case of Lactobacillus kefiranofaciens, Roche 454 GS FLX pyrosequencing technology was combined with Illumina Genome Analyzer IIx Solexa high throughput sequencing technology to sequence the genome ³¹.

In most cases, genome assembly was done using different versions of Newbler assembler ^{33, 39} except in a few cases where gsAssembler ^{36, 37} or CLC Genomics Workbench ³⁷ Phred-Phrap-Consed software package ⁴¹. Genome annotation was done using the Rapid Assembly using Subsystems Technology (RAST) server ^{38 - 40}, often combined with Glimmer ³⁸, tRNAscan-SE ³⁸, RNAmmer³⁸, EDGAR³⁶, PEDANT ⁴¹, GeneMark ⁴¹, and NCBI Prokaryotic Genome Automated Annotation Pipeline (PGAAP) analysis ^{33, 36}.

The following year also had several probiotic genomes including those of Lactobacillus rhamnosus ²⁶, Lactobacillus vini ⁴², Lactobacillus curvatus ³², Lactobacillus fructivorans ⁴³, and Lactobacillus helveticus ⁴⁴ were sequenced using the Roche 454 GS FLX Titanium pyrosequencing technology, while the genome of Lactobacillus rossiae ³⁴ was sequenced using the Illumina HiSeq 2000 platform. Even here, genome assembly was predominantly carried done using Newbler Assembler with the exception of the use of whole genome sequence assembler (wgs Assembler), genome sequence assembler (gsAssembler) and GS Reference Mapper for the assembly of Lactobacillus helveticus, Lactobacillus vini, and Lactobacillus rhamnosus genomes respectively ^{26, 42, 44}. Genome annotation was done by similar software that was mentioned before with RAST and PGAAP being the predominant tools for annotation.

In 2013, probiotic genome sequencing witnessed a more heterogeneous usage of sequencing platforms with the Applied Biosystems ABI377 and 3700 automated sequencers ⁴⁵, and the Ion Torrent Personal Genome Machine ⁴⁶ entering the arena where Roche 454 GS FLX ⁴⁷, Illumina Genome Analyzer Iix ⁴⁸, and Illumina HiSeq 2000 ⁴⁹ existed. The species whose genomes were sequenced in this period include Lactobacillus pentosus ⁴⁸, Lactobacillus helveticus ⁴⁵, Lactobacillus shenzhenensis ⁴⁹, Lactobacillus ginsenosidimutans ⁵⁰, Lactobacillus florum ⁵¹, Lactobacillus pobuzihii ⁵², Lactobacillus jensenii, Lactobacillus gasseri ⁴⁶, and Lactobacillus otakiensis ⁴⁷. Additionally, with heterogeneous usage of sequencing technologies came the usage of multiple assembly and annotation software. While most sequences that came out of Roche 454 GS FLX platform were assembled by different versions of Newbler ⁴⁷, sequence from Ion Torrent PGM were assembled using Ion Torrent Assembler ⁴⁶ or CLC de Novo Genomics Workbench, while the output from Illumina platforms were assembled using SOAP deNovo ⁴⁹ or Velvet ⁴⁸ software. Annotation was predominantly done by RAST and PGAAP analysis, but ERGO, GTPS, RDP, Silva, and ERGO were the new additions to the group ^{45, 47}.

The year 2014 witnessed an increased use of Illumina and Ion Torrent platforms for sequencing probiotic genomes. While genomes of Lactobacillus mucosae ⁵³, Lactobacillus sakei ⁵⁴, Bifidobacterium moukalabense ⁵⁵, Lactobacillus sucicola ⁵⁶, Lactobacillus farraginis ⁵⁷, and Lactobacillus composti ⁵⁷ were sequenced using Ion Torrent Personal Genome Machine, the genomes of Lactobacillus equi ⁵⁸, Lactobacillus animalis ⁵⁹, Lactobacillus oryzae, Lactobacillus fabifermentans ⁶⁰, and Lactobacillus salivarius ⁶¹ were sequenced by Illumina platforms. Roche 454 GS FLX pyrosequencer was used to sequence Lactobacillus gasseri and Lactobacillus namurensis ⁶² genomes.

In case of genome assembly, there was a diverse use of assembly software that was perhaps used to match the requirements of a particular genome. While genomes sequenced using Roche 454 GS FLX continued to be assembled using Newbler assembler ⁶², genomes sequenced using Ion Torrent systems were assembled using Newbler ⁵⁷, NGen (DNAStar) ⁵³, or CLC Genomics Workbench ⁵⁴, and reads from Illumina platforms used Abyss^{61, 63}, Velvet ^{59, 63}, Platanus ⁶⁰, AMOS ⁵⁹, Hawkeye ⁵⁹ either in isolation or in concert. RAST server and PGAAP continued to be the predominant annotation platform, newer tools like GAMOLA⁵⁹, MetaGene Annotator ⁶⁰, MiGAP ⁶⁰, SignalP ⁶¹, InterPro ⁶¹, TMHMM ⁶¹, and Artemis being used for annotation and curation.

In the next two years, a number of probiotic species were sequenced. The year 2015 not only witnessed the use of all types of sequencing technologies, but also witnessed the combinatorial use of many of them. The combinations were either a combination of Roche 454 pyrosequencers with Illumina platforms ⁶⁴ or with Sanger sequencing methods ⁶⁵. Single molecule real time (SMRT) Pacific Biosciences RSII sequencer was another technology that was used this year ⁶⁶. The species that were sequenced during this year include Lactobacillus delbrueckii ⁶⁷, Bifidobacterium catenulatum ⁶⁸, Bifidobacterium pseudolongum⁶⁶, Lactobacillus johnsonii ²⁹, Lactobacillus rhamnosus ⁶⁹, Lactobacillus reuteri ⁷⁰, Bifidobacterium angulatum ⁷¹, Bifidobacterium adolescentis ⁷¹, Lactobacillus kunkeei ⁷², Lactobacillus mucosae ⁶⁴, Bifidobacterium scardovii ⁶⁵, Bifidobacterium aesculapii ⁷³, Lactobacillus curieae ⁷⁴, Lactobacillus acidophilus ⁷⁵, Bifidobacterium actinocoloniiforme ⁷⁶, Lactobacillus curvatus ⁷⁷, Lactobacillus rhamnosus ⁶⁹, Lactobacillus fermentum ^{78, 79}, Bifidobacterium kashiwanohense ^{80, 81}, Lactobacillus paracasei ⁸², Lactobacillus hokkaidonensis ⁸³, and Lactobacillus farciminis ⁸⁴. The assemblers used included Newbler ⁷², Velvet ²⁹, gs Assembler ⁷¹, CLC Genomics Workbench ⁸⁵, SOAP deNovo⁷⁴, SPAdes ⁸⁶,  Ngen ⁶⁷, and Phred-Phrap-Consed ⁶⁸ as seen in the previous years and annotation was done mostly using RAST server and PGAAP pipeline ⁸⁵, complemented with Glimmer, tRNAscan-SE, Prodigal, GenePRIMP ^{65, 72}. One of the new assemblers used in this year was MIRA ⁶⁴. 

In 2016 also, several probiotic genomes have been sequenced mainly using Illumina platforms ⁸⁷ with isolated use of Ion Torrent ⁸⁸, Pacific BioSciences ³⁵ and Roche 454 ³⁰ platforms as well. The probiotics that have been sequenced this year include Lactobacillus casei ^{30, 87}, Lactobacillus sakei ⁸⁹, Lactobacillus plantarum ^{88, 90, 91}, Lactobacillus equigenerosi ⁹², Lactobacillus crispatus ⁹³, Lactobacillus kunkeei ³⁵, Bifido bacterium longum ⁹⁴, Lactobacillus farciminis ⁹⁵, Lactobacillus johnsonii ⁹⁶, Lactobacillus brevis ⁹⁷, and Lactobacillus collinoides ⁹⁸. Genome assemblies were mostly done with the help of software like Newbler ⁹², Ngen ⁹¹, SOAP deNovo ⁹⁶, SPAdes ⁸⁸, Abyss ⁹⁴, Ray Assembler ⁹⁰, and CLC Genomics Workbench ⁸⁷. Annotation was predominantly done using RAST server and PGAAP pipeline ⁹¹ with the additional use of Glimmer, tRNAscan-SE, and RNAmmer ⁹¹.

With the explosive amount of genomic data generated in the recent year, efforts towards their analyses have also been slowly progressing. The last two years have seen several comparative genomic analyses of the strains belonging to the aforementioned genera of probiotics ^{99 - 101}.

Furthermore, in the recent years, a special interest is also observed in studies pertinent to carbohydrate utilization in these organisms ¹⁰². Also, there has been an impetus for the identification of novel genes helpful in diagnostics ¹⁰³, and genomic characterization of important traits like motility⁷⁷.

TABLE 1: SPECIES, TYPE OF GENOME SEQUENCE AND TECHNOLOGY USED

CONCLUSION: In conclusion, the application of genomic technologies in probiotic research has facilitated better understanding of probiotic bacteria and the genes and the molecular mechanisms that endow them with characteristic traits. The advances in sequencing technologies through the years, represented by the four generations of high throughput sequencing technologies, have eventually enabled easier and faster acquisition of genome data as seen by the reports of the genome sequences published over the years. A parallel advance has also been witnessed in the development of genome assembly and annotation software and tools to facilitate the analysis of the genome data. Furthermore, studies pertinent to the biomolecule utilization and comparative genomics studies of probiotic genomes have been gaining momentum in the recent years.

Future Work: As understanding complete genome maps of probiotic bacteria give us insights into the characteristic traits of particular species, it is important to analyze and understand the genomes of these probiotics. It is also crucial that we look deeper into the genome to see what they actually possess. Comparative Genomics studies have to be carried out as they could reveal genes that are critical in rendering the probiotics non-pathogenic, distinguishing them from the other bacteria. This will also help us connect the similar traits present in different probiotic species, helping us understand the evolutionary relationship among the bacterial communities that form the intestinal microbiota. It is therefore, the need of the hour to develop databases and tools that aid in the analysis of probiotic genomes through comparative genomics studies.

ACKNOWLEDGEMENT: The author would like to acknowledge the support of Department of Genetic Engineering, SRM University.

CONFLICT OF INTEREST: The author has no conflict of interest to declare.

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     How to cite this article:

     Joseph JP: Probiotic genomes: sequencing and annotation in the past decade. Int J Pharm Sci Res 2018; 9(4):1351-62.doi:10.13040/ IJPSR.0975-8232.9(4).1351-62.

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