by Kelly Lagor
Kelly Lagor discusses the ongoing microbial threats to the global citrus industry, which she links to her favorite poem and her latest story, “As Ordinary Things Often Do,” from our [January/February issue, on sale now!]
You may have noticed citrus has gotten more expensive lately. It’s due, in part to the intense El Nino weather patterns from the last five years, which have caused damaging storms, disruptions of the hydrological cycles, and higher temperatures. Matters, however, are not being helped by the devastating plant disease known as Huanglongbing, aka citrus greening, that the USDA has called “the most serious threat to the US citrus industry in history.” All varieties of citrus trees in the world can be impacted, and citrus greening has caused the collapse of citrus industries in Asia and Africa. Affected plants display a hallmark yellow mottling of their leaves, stunted growth, premature flowering and leaf loss; and they produce small fruit with a half-green rind (even after ripening) that have a bitter taste. After a few years of steadily declining crop yields and worsening health, affected trees die.
Citrus greening is a two-fold problem. First, the disease is caused by three species of bacteria in the genus Liberibacter. All thrive in warmer temperatures, like those found in regions where citrus grows best, such as in Brazil, southern China, India, and across the southern US, but it’s the warm temperature-tolerant Asian (L. asiaticus) species that’s been responsible for the widespread damage to global citrus crops. Furthermore, warming temperatures due to climate change have lengthened the season in which these bacteria grow best, making them harder to control. Once in a plant, Liberibacter colonize the plant’s nutritionally rich phloem vasculature, causing clogs as they become nutritional sinks as they multiply, which further prevents the plant from efficiently distributing nutrients to all its tissues.
Second, the bacteria spreads from tree to tree via insect vectors. Gnat-sized species in the Psyllidae family (also known as the “jumping plant lice”) feed on the sugar-rich sap in the phloem of specific species of plants. In the case of the Asian citrus psyllid (Diaphorina citri), if a plant they’re feeding on is infected by L. asiaticus, they ingest the bacteria along with the sap. The bacteria then colonize their salivary glands, which can happen after as little as fifteen minutes of feeding. Once established in a psyllid, the bacteria persist for life, allowing the insect to infect every subsequent plant it feeds upon.
L. asiaticus has proven difficult to study. It is an obligate parasite, reflected in its small genome that’s lost many genes involved in making things like essential amino acids, which it gets instead from its hosts. This means it can’t be grown outside of either its plant or insect host, stymying attempts to understand how it evades plant immunity and how infections might be effectively treated or prevented. Recent breakthroughs, thanks to newer methods of bacterial enrichment from infected plant samples, as well as the cheaper cost of DNA sequencing, however, have enabled the first profiling experiments of L. asiaticus’ transcriptome and metabolome earlier in 2024.
Li et al’s* multiomic approach revealed how L. Asiaticus may be suppressing a plant’s innate immunity to biotrophic pathogens by suppressing the programmed cell death a plant triggers to kill infected tissues to prevent such pathogens from reproducing and spreading. They also identified L. asiaticus’ method of movement, how it likely adheres to host tissues, what kind of feeding methods it uses, and a CRISPR/cas system L. asiaticus uses to protect itself from bacteriophages. They also identified a likely reason why infected plants become stunted and eventually die, as the bacteria preferentially metabolize only some plant-produced sugars, leaving others to accumulate in the plant’s leaves, which inhibits photosynthesis. The phloem blockages it causes also cause those same sugars to accumulate in the fruit’s pith, rather than the fruit itself. That so much can be deduced from just the sequencing of L. asiaticus’ genome andRNA is thanks to the foundational work microbiologists have done over the last twenty years both sequencing and characterizing various microbial species, and their survival and metabolism strategies.
Since the first cases identified in Florida in 2005, citrus greening has been found in citrus crops across many regions of the southern US, all the way to California. Current mitigations are the use of quarantine (which covers entire impacted regions and states); the use of insecticides to control psyllid populations (which become less effective over time as insects evolve under their selection pressure); and approaches like injecting infected trees with antibiotics, which raises the risk of further antibiotic resistance genes arising, causes damage to the plant and it’s immediate ecology’s microbiome, which causes longer term damage to the plant and the ecosystem. Intense research is being done to identify biological methods to control L. asiaticus. No naturally immune cultivars have yet been identified, so such methods must be built from the ground up.
Research like the above, as well as newer tools for genetically altering crop plants, such as CRISPR, means we’re better able than ever to intervene in such agricultural problems the Anthropocene is bringing about. Citrus greening is just one of many ways in which globalized trade and climate change is destabilizing agriculture in unpredictable and difficult to address ways. How will increased temperatures, changing water availability, and increased carbon dioxide concentrations affect other microbial species in the world? Microbes are largely responsible for the nutrient cycles – like of nitrogen, carbon, and sulfur – that all life depends on – will human activity destabilize these cycles? How will microbes responsible for these processes respond? Will we be able to intervene in time again to avert disaster, just like we are attempting to do with citrus greening?
While microbes evolve via small genetic changes over time, they also rapidly acquire new traits from the microbes around them, thanks to the large amount of gene swapping microbes do, via things like conjugation, infection with bacteriophages toting extra genes around they stole from their last host, or even by picking up stray DNA from the environments. This means microbial populations can be quick to adapt to changing conditions around them. Does this mean that microbes might have a buffering effect on global warming? Or might they instead amplify it? Right now, with our limited understanding of microbial genetics and diversity, it is impossible to say. To give an idea of just how much we don’t know about this dominant form of life on earth (microbes were the only game in town from about 700 million years after the earth formed 4.5 billion years ago, up until about 600 million years ago when multicellular life was made possible thanks to all the oxygen pumped out by cyanobacteria), just twenty years ago, estimates of microbial diversity predicted one million species of bacteria. Today, that number is maybe one trillion species, and we know a lot about maybe 10,000 of those species.
Rhoda is a microbiologist in “As Ordinary Things Often Do” because in the next few centuries, the importance of work being done by microbiologists, like the scientists above working on problems like citrus greened, can’t be understated. We’ll need them to help understand an abate countless ecological and agricultural disasters we have in store. We’ll need them to help develop new biological tools that might even be able to help reverse some of the worst climate change predictions. If we do happen to soon find a planet in our stellar neighborhood that shows spectrographic signs of life, we’ll need microbiologists to help get us to that planet alive and healthy, and we’ll absolutely need them to understand the nature of what is likely the dominant form of life on that planet as well.
Why the long aside above about oranges? It’s because I named my story after a line in the poem “The Orange” by Wendy Cope (see below). It’s a simple poem about life’s simple pleasures. Such pleasures, like the joy of splitting a huge orange with your friends will hopefully be possible for at least a few more years, if not decades. But what about after that? What happens if we keep pretending like climate change isn’t happening? Maybe days with such a feeling of ease, like the one Cope beautifully captures in her poem, might becoming even more precious than they already are.
So maybe go buy some expensive oranges from your beleaguered local growers, encourage young people in your life to go into science, figure out little things you and your friends and family and neighbors can do to help with climate change locally, and find all the enjoyment you can in the little things in the meantime.
The Orange
By Wendy Cope
At lunchtime I bought a huge orange –
The size of it made us all laugh.
I peeled it and shared it with Robert and Dave-
They got quarters and I had a half.
And that orange, it made me so happy,
As ordinary things often do
Just lately. The shopping. A walk in the park.
This is peace and contentment. It’s new.
The rest of the day was quite easy.
I did all the jobs on my list
And enjoyed them and had some time over.
I love you. I’m glad I exist.
*Li Y, Ma R, Gao C, Li Z, Zheng Y, Fang F, Wang C, Li G, Du X, Xu C, Xu M, Liu R, Deng X, Zheng Z. Integrated bacterial transcriptome and host metabolome analysis reveals insights into “Candidatus Liberibacter asiaticus” population dynamics in the fruit pith of three citrus cultivars with different tolerance. Microbiol Spectr. 2024 Apr 2;12(4):e0405223. doi: 10.1128/spectrum.04052-23. Epub 2024 Mar 5. PMID: 38440971; PMCID: PMC10986616.
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