Biological invasions alter environmental microbiomes: A meta-analysis

Malacrinò, Antonino; Sadowski, Victoria A; Martin, Tvisha; Oliveira, Nathalia Cavichiolli de; Brackett, Ian J.; Feller, James D.; Harris, Kira; COMBITA-HEREDIA, ORLANDO; Vescio, Rosa; Bennett, Alison E.

doi:10.1371/journal.pone.0240996

Cited by 14 publications

(11 citation statements)

References 82 publications

(132 reference statements)

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“…Both bacterial and fungal communities varied among plant communities in the experimental plots, supporting previous work showing that invasive plants change microbial communities in predictable ways (e.g. Gibbons et al, 2017;Lekberg et al, 2013;Malacrinò et al, 2020). Whether microbial communities respond directly to differences in plant traits, phenology and life history here, or indirectly to invader-mediated shifts in soil edaphic conditions is unknown.…”

Section: Invasions Change Fungal and Bacterial Communities And Changes Are Invader Specificsupporting

confidence: 79%

The effect of plant invasion on soil microbial carbon‐use efficiency in semi‐arid grasslands of the Rocky Mountain West

Nasto

McLeod²,

Bullington

et al. 2021

Journal of Ecology

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1. Grassland ecosystems invaded by exotic plant species often exhibit substantially higher above-ground productivity and soil nitrogen (N) than the native communities they replace. These shifts are likely associated with altered microbial carbon (C) and N cycling, but we know surprisingly little about how these processes change with plant invasion.2. Targeting four invasive plant species common in the Rocky Mountain West, we collected soils from invaded and adjacent uninvaded grassland field plots, as well as from an experimental garden. We used a laboratory incubation of soils with 13 C-and 15 N-labelled substrates to examine how microbial C respiration, C assimilation and N cycling differed among plant communities. To assess how these rates corresponded with plant productivity and microbial communities, we measured above-ground plant biomass and characterized bacterial and fungal communities using Illumina sequencing.3. In the paired observational plots, soil microbial communities associated with invaders generally had higher respiration rates and lower growth rates than those associated with the native plant communities, leading to a lower microbial carbon-use efficiency (CUE). Overall, soil substrate with a lower C:N was related to decreased CUE, and lower CUE was related to increased gross and net N mineralization. In turn, faster gross N mineralization was related to greater aboveground biomass. These patterns coincided with significant differences in fungal communities, whereas bacterial communities varied by site. Invasive plants also altered microbial communities in the experimental plots, but this was not associated with shifts in microbial CUE, which was low overall. Synthesis.Our results provide evidence that invasive plants alter bacterial and fungal communities. These shifts were not associated with changes in microbial CUE and, thus, the often-assumed link between compositional and functional shifts was not apparent in this study. However, lower CUE was associated with elevated rates of N cycling and productivity, which, in low-productivity systems, could help explain the increased growth and success of exotic plant invaders.

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Section: Invasions Change Fungal and Bacterial Communities And Changes Are Invader Specificsupporting

confidence: 79%

The effect of plant invasion on soil microbial carbon‐use efficiency in semi‐arid grasslands of the Rocky Mountain West

Nasto

McLeod²,

Bullington

et al. 2021

Journal of Ecology

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“…In addition to negative effects on biodiversity, the economy, and human health, biological invasions may drive emergence of (new) diseases and changes in diversity and structure of microbial populations in the novel environment and may also affect population dynamics of invasive species ( 5 , 35 ). Here, we analyzed differences in the microbiomes of different tissues of the successful freshwater invader the signal crayfish.…”

Section: Discussionmentioning

confidence: 99%

“…The contribution of the microbiota in maintaining individual health and resilience of animal populations in the wild is being increasingly recognized ( 1 ) as well as its role in the context of biological invasions ( 2 – 5 ). Invasive alien species (IAS) are species that have been introduced either accidentally or intentionally outside their natural range and whose introduction and spread has negative effects on biodiversity, the economy, or human health in the new environment ( 6 ).…”

Section: Introductionmentioning

confidence: 99%

“…Recent research demonstrated the effects of IAS on microbial communities in the novel environment. For example, biological invasions affect ecosystem functions, which may consequently drive changes in diversity and shifts in structure of environmental microbial populations (e.g., microbial diversity loss) ( 1 , 5 ). Also, transmission of novel microbial pathogens is considered one of the main mechanisms through which IAS outcompete their native counterparts and pose a threat to human, animal, and ecosystem health ( 4 , 10 ).…”

Section: Introductionmentioning

confidence: 99%

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Microbiome of the Successful Freshwater Invader, the Signal Crayfish, and Its Changes along the Invasion Range

et al. 2021

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Invasive species are among the major drivers of biodiversity loss and impairment of ecosystem services worldwide, but our understanding of their invasion success and dynamics still has many gaps. For instance, although it is known that host-associated microbial communities may significantly affect an individual’s health and fitness, the current studies on invasive species are mainly focused on pathogenic microbes, while the effects of the remaining majority of microbial communities on the invasion process are almost completely unexplored.

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“…Invasive species potentially alter microbes present in their introduced environment [14], or the microbiomes of native species [15], and may harbor symbionts that allow these invasive species to exploit new resources [16]. Hymenoptera are often exposed to microbes through environmental contact [17][18][19], vertical transmission [20], or social transfer between nestmates [21,22].…”

Section: Introductionmentioning

confidence: 99%

Microbiome of the wasp Vespula pensylvanica in native and invasive populations, and associations with Moku virus

et al. 2021

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Invasive species present a worldwide concern as competition and pathogen reservoirs for native species. Specifically, the invasive social wasp, Vespula pensylvanica, is native to western North America and has become naturalized in Hawaii, where it exerts pressures on native arthropod communities as a competitor and predator. As invasive species may alter the microbial and disease ecology of their introduced ranges, there is a need to understand the microbiomes and virology of social wasps. We used 16S rRNA gene sequencing to characterize the microbiome of V. pensylvanica samples pooled by colony across two geographically distinct ranges and found that wasps generally associate with taxa within the bacterial genera Fructobacillus, Fructilactobacillus, Lactococcus, Leuconostoc, and Zymobacter, and likely associate with environmentally-acquired bacteria. Furthermore, V. pensylvanica harbors—and in some cases were dominated by—many endosymbionts including Wolbachia, Sodalis, Arsenophonus, and Rickettsia, and were found to contain bee-associated taxa, likely due to scavenging on or predation upon honey bees. Next, we used reverse-transcriptase quantitative PCR to assay colony-level infection intensity for Moku virus (family: Iflaviridae), a recently-described disease that is known to infect multiple Hymenopteran species. While Moku virus was prevalent and in high titer, it did not associate with microbial diversity, indicating that the microbiome may not directly interact with Moku virus in V. pensylvanica in meaningful ways. Collectively, our results suggest that the invasive social wasp V. pensylvanica associates with a simple microbiome, may be infected with putative endosymbionts, likely acquires bacterial taxa from the environment and diet, and is often infected with Moku virus. Our results suggest that V. pensylvanica, like other invasive social insects, has the potential to act as a reservoir for bacteria pathogenic to other pollinators, though this requires experimental demonstration.

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Biological invasions alter environmental microbiomes: A meta-analysis

Cited by 14 publications

References 82 publications

The effect of plant invasion on soil microbial carbon‐use efficiency in semi‐arid grasslands of the Rocky Mountain West

The effect of plant invasion on soil microbial carbon‐use efficiency in semi‐arid grasslands of the Rocky Mountain West

Microbiome of the Successful Freshwater Invader, the Signal Crayfish, and Its Changes along the Invasion Range

Microbiome of the wasp Vespula pensylvanica in native and invasive populations, and associations with Moku virus

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