Evolutionary Ecology of Prokaryotic Immune Mechanisms

Houte, Stineke van; Buckling, Angus; Westra, Edze R.

doi:10.1128/mmbr.00011-16

Cited by 223 publications

(189 citation statements)

References 266 publications

(329 reference statements)

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“…Consistent with this scenario, the evolutionary loss of motility from bacteria reared on homogenous media in the laboratory is common (Fux, Shirtliff, Stoodley, & Costerton, ; Sellek et al., ), and the cycling of bacteria between fly and food has been demonstrated empirically for Acetobacter isolated from laboratory Drosophila (Blum, Fischer, Miles, & Handelsman, ). These effects may be compounded by selection for nonmotility exerted by certain bacteriophage that utilize the flagellum as receptor (van Houte, Buckling, & Westra, ) and the energetic costs of the proton motive force required for motility (Edwards, Sockett, & Brookfield, ; Koskiniemi, Sun, Berg, & Andersson, ). Interestingly, the host immune system is unlikely to be a factor selecting against motility because, although the bacterial flagellin protein is recognized by the immune system of many animals and plants, Drosophila and other insects apparently lack the receptors that recognize this protein (Buchon, Silverman, & Cherry, ).…”

Section: Discussionmentioning

confidence: 99%

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

et al. 2017

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Various bacterial taxa have been identified both in association with animals and in the external environment, but the extent to which related bacteria from the two habitat types are ecologically and evolutionarily distinct is largely unknown. This study investigated the scale and pattern of genetic differentiation between bacteria of the family Acetobacteraceae isolated from the guts of Drosophila fruit flies, plant material and industrial fermentations. Genome-scale analysis of the phylogenetic relationships and predicted functions was conducted on 44 Acetobacteraceae isolates, including newly-sequenced genomes from 18 isolates from wild and laboratory Drosophila. Isolates from the external environment and Drosophila could not be assigned to distinct phylogenetic groups, nor are their genomes enriched for any different sets of genes or category of predicted gene functions. In contrast, analysis of bacteria from laboratory Drosophila showed they were genetically distinct in their universal capacity to degrade uric acid (a major nitrogenous waste product of Drosophila) and absence of flagellar motility, while these traits vary among wild Drosophila isolates. Analysis of the competitive fitness of Acetobacter discordant for these traits revealed a significant fitness deficit for bacteria that cannot degrade uric acid in culture with Drosophila. We propose that, for wild populations, frequent cycling of Acetobacter between Drosophila and the external environment prevents genetic differentiation by maintaining selection for traits adaptive in both the gut and external habitats. However, laboratory isolates bear the signs of adaptation to persistent association with the Drosophila host under tightly-defined environmental conditions.

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Section: Discussionmentioning

confidence: 99%

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

et al. 2017

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“…For a small fraction of the spacers, protospacers have been reported, often in viral and plasmid genomes, but the substantial majority of the spacers remain without a match, representing vast CRISPR "dark matter" (43)(44)(45)(46)(47)(48)(49).…”

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confidence: 99%

The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes

Shmakov

Sitnik

Makarova

et al. 2017

mBio

202

195

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Clustered regularly interspaced short palindromic repeats and CRISPRassociated protein (CRISPR-Cas) systems store the memory of past encounters with foreign DNA in unique spacers that are inserted between direct repeats in CRISPR arrays. For only a small fraction of the spacers, homologous sequences, called protospacers, are detectable in viral, plasmid, and microbial genomes. The rest of the spacers remain the CRISPR "dark matter." We performed a comprehensive analysis of the spacers from all CRISPR-cas loci identified in bacterial and archaeal genomes, and we found that, depending on the CRISPR-Cas subtype and the prokaryotic phylum, protospacers were detectable for 1% to about 19% of the spacers (~7% global average). Among the detected protospacers, the majority, typically 80 to 90%, originated from viral genomes, including proviruses, and among the rest, the most common source was genes that are integrated into microbial chromosomes but are involved in plasmid conjugation or replication. Thus, almost all spacers with identifiable protospacers target mobile genetic elements (MGE). The GC content, as well as dinucleotide and tetranucleotide compositions, of microbial genomes, their spacer complements, and the cognate viral genomes showed a nearly perfect correlation and were almost identical. Given the near absence of self-targeting spacers, these findings are most compatible with the possibility that the spacers, including the dark matter, are derived almost completely from the species-specific microbial mobilomes. IMPORTANCEThe principal function of CRISPR-Cas systems is thought to be protection of bacteria and archaea against viruses and other parasitic genetic elements. The CRISPR defense function is mediated by sequences from parasitic elements, known as spacers, that are inserted into CRISPR arrays and then transcribed and employed as guides to identify and inactivate the cognate parasitic genomes. However, only a small fraction of the CRISPR spacers match any sequences in the current databases, and of these, only a minority correspond to known parasitic elements. We show that nearly all spacers with matches originate from viral or plasmid genomes that are either free or have been integrated into the host genome. We further demonstrate that spacers with no matches have the same properties as those of identifiable origins, strongly suggesting that all spacers originate from mobile elements.KEYWORDS CRISPR-Cas, bacteriophages, mobilome, oligonucleotide composition, spacer acquisition C RISPR-Cas (clustered regularly interspaced palindromic repeats and CRISPRassociated proteins) systems are adaptive (acquired) immune systems of archaea and bacteria that store memory of past encounters with foreign DNA in unique spacer Citation Shmakov SA, Sitnik V, Makarova KS, Wolf YI, Severinov KV, Koonin EV. 2017. The CRISPR spacer space is dominated by sequences from species-specific mobilomes.

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“…Well-known systems include restriction-modification, CRISPR-Cas, abortive infection, prokaryotic Argonaute, and the recently discovered BREX [14–17] (Figure 2B). Of these, restriction-modification systems are the most prevalent, appearing in approximately 95% of all sequenced bacterial genomes [18], and commonly are considered the greatest barrier to DNA transfer.…”

Section: Delivering and Maintaining Exogenous Dnamentioning

confidence: 99%

Toward a genetic tool development pipeline for host-associated bacteria

Waller

Bober

Nair

et al. 2017

Current Opinion in Microbiology

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Bacteria reside in externally accessible niches on and in multicellular organisms, often forming mutualistic relationships with their host. Recent studies have linked the composition of these microbial communities with alterations in the host’s health, behavior, and development, yet the causative mediators of host-microbiota interactions remain poorly understood. Advances in understanding and engineering these interactions require the development of genetic tools to probe the molecular interactions driving the structure and function of microbial communities as well as their interactions with their host. This review discusses the current challenges to rendering culturable, non-model members of microbial communities genetically tractable--including overcoming barriers to DNA delivery, achieving predictable gene expression, and applying CRISPR-based tools--and details recent efforts to create generalized pipelines that simplify and expedite the tool-development process. We use the bacteria present in the human gastrointestinal tract as representative microbiota to illustrate some of the recent achievements and future opportunities for genetic tool development.

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Evolutionary Ecology of Prokaryotic Immune Mechanisms

Cited by 223 publications

References 266 publications

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

A genomic investigation of ecological differentiation between free‐living and Drosophila‐associated bacteria

The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes

Toward a genetic tool development pipeline for host-associated bacteria

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