The first 1000 cultured species of the human gastrointestinal microbiota

Abstract

The microorganisms that inhabit the human gastrointestinal tract comprise a complex ecosystem with functions that significantly contribute to our systemic metabolism and have an impact on health and disease. In line with its importance, the human gastrointestinal microbiota has been extensively studied. Despite the fact that a significant part of the intestinal microorganisms has not yet been cultured, presently over 1000 different microbial species that can reside in the human gastrointestinal tract have been identified. This review provides a systematic overview and detailed references of the total of 1057 intestinal species of Eukarya (92), Archaea (8) and Bacteria (957), based on the phylogenetic framework of their small subunit ribosomal RNA gene sequences. Moreover, it unifies knowledge about the prevalence, abundance, stability, physiology, genetics and the association with human health of these gastrointestinal microorganisms, which is currently scattered over a vast amount of literature published in the last 150 years. This detailed physiological and genetic information is expected to be instrumental in advancing our knowledge of the gastrointestinal microbiota. Moreover, it opens avenues for future comparative and functional metagenomic and other high-throughput approaches that need a systematic and physiological basis to have an impact.

Keywords: diversity; function; gastrointestinal; gut; microbiome; microbiota.

Fig 1

Graphical representation of the cumulative number of cultured species from Bacteria, Archaea and Eukarya from the human gastrointestinal tract as a function of time. The arrows indicate the turning points of the gastrointestinal microbiota research: (1) Isolation of the first gastrointestinal bacterial species, (2) Introduction of strictly anaerobic techniques, and (3) Introduction of molecular techniques in the field of the gastrointestinal microbiota research.

Fig 2

Phylogenetic tree of the human gastrointestinal microbiota. The numbers in parentheses indicate the number of cultured species given per phylum. The pie charts illustrate distribution between the number of species with full genome sequence genome (full sectors), the number of species with partial genome sequence (semi-full sectors) and number of species without any genome sequence (empty sectors) given for Archaea, Eukarya and per phylum for Bacteria. The color code of pies corresponds to the color code of the phylogenetic tree.

Fig 3

Phylogenetic tree of the human gastrointestinal species that belong to the orders of the Bifidobacteriales and Coriobacteriales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 4

Phylogenetic tree of a fraction of the human gastrointestinal species that belong to the order of the Actinomycetales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. For the other human gastrointestinal species that cluster within the Actinomycetales see Fig. 5.

Fig 5

Phylogenetic tree of a fraction of the human gastrointestinal species that belong to the order of the Actinomycetales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. For the other human gastrointestinal species that cluster within the Actinomycetales see Fig. 4.

Fig 6

Phylogenetic tree of the human gastrointestinal species that belong to the class of the Bacteroidia. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. Deeply rooted Bacteroides spp., which based on the SSU rRNA gene sequence cluster within distant phylogenetic groups are depicted in the gray area.

Fig 7

Phylogenetic tree of the human gastrointestinal species that belong to the classes of the Cytophagia and Sphingobacteria. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 8

Phylogenetic tree of a fraction of the human gastrointestinal species that belong to the order of the Lactobacillales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. For the other gastrointestinal species that belong to the order of the Lactobacillales see Fig. 9.

Fig 9

Phylogenetic tree of the human gastrointestinal species that belong to the families of Streptococcaceae and Enterococcaceae. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. For the other gastrointestinal species that belong to the order of the Lactobacillales see Fig. 8.

Fig 10

Phylogenetic tree of a fraction of the human gastrointestinal species that belong to the order of the Bacillales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification. For the other gastrointestinal species that belong to the order of the Bacillales see Fig. 11.

Fig 11

Phylogenetic tree of a fraction of the human gastrointestinal species that belong to the order of the Bacillales. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. For the other gastrointestinal species that belong to the order of the Bacillales order see Fig. 10.

Fig 12

Phylogenetic tree the human gastrointestinal species that belong to the family of Clostridiaceae. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification. Deeply rooted Clostridium spp., which based on the SSU rRNA gene sequence cluster within distant phylogenetic groups, are depicted in the gray area.

Fig 13

Phylogenetic tree the human gastrointestinal species that belong to the family of the Lachnospiraceae. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification.

Fig 14

Phylogenetic tree the human gastrointestinal species that belong to the Clostridium cluster IV, most of which belong to the family of the Ruminococcaceae. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification. Deeply rooted Ruminococcus spp., which based on the SSU rRNA gene sequence cluster within distant phylogenetic groups, are depicted in the gray area.

Fig 15

Phylogenetic tree the human gastrointestinal species that belong to the family of the Eubacteriaceae and Clostridiales Family XIII Incertae Sedis. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification. Deeply rooted Eubacterium spp., which based on the SSU rRNA gene sequence cluster within distant phylogenetic groups are depicted in the gray area.

Fig 16

Phylogenetic tree the human gastrointestinal species that belong to families of the Peptostreptococcaceae and Clostridiales Family XI Incertae Sedis. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification.

Fig 17

Partially opened phylogenetic tree the human gastrointestinal species that belong to the Firmicutes phylum on which five species that cluster within the three families with low diversity are indicated.

Fig 18

Phylogenetic tree the human gastrointestinal species that belong to the order of the Negativicutes. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 19

Phylogenetic tree the human gastrointestinal species that belong to the order of the Erysipelotrichi. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species, while the family is divided over Clostridium clusters (Collins et al., 1994). The species indicated in bold are based on the SSU rRNA gene sequence clustering within the Erysipelotrichi in contrast to their official classification.

Fig 20

Phylogenetic tree the human gastrointestinal species that belong to the phylum of the Fusobacteria. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold are based on the SSU rRNA gene sequence clustering within the families that are designated on the figure in contrast to their official classification.

Fig 21

Phylogenetic tree the human gastrointestinal species that belong to the class of the Alphaproteobacteria class. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 22

Phylogenetic tree the human gastrointestinal species that belong to the class of the Betaproteobacteria. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 23

Phylogenetic tree the human gastrointestinal species that belong to the family of the Enterobacteriaceae. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 24

Phylogenetic tree the human gastrointestinal species that belong to the class of the Gammaproteobacteria without Enterobacteriaceae family. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated.

Fig 25

Phylogenetic tree the human gastrointestinal species that belong to the classes of the Deltaproteobacteria and Epsilonproteobacteria. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the family names are indicated. The species indicated in bold is based on the SSU rRNA gene sequence clustering within the indicated family in contrast to its official classification.

Fig 26

Phylogenetic tree the human gastrointestinal species that belong to the different bacterial phyla with limited diversity, and two archaeal phyla. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the phylum names are indicated.

Fig 27

Phylogenetic tree the human gastrointestinal Fungi. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the phylum names are indicated.

Fig 28

Phylogenetic tree the human gastrointestinal microeukarya. GenBank Accession Numbers of the SSU rRNA gene sequence are provided for each species and the phylum names are indicated.